Fsufs 05 606815

REVIEW
published: 19 February 2021

doi: 10.3389/fsufs.2021.606815
Rethinking Crop Nutrition in Times of

Modern Microbiology: Innovative
Biofertilizer Technologies
Eduardo K. Mitter 1 , Micaela Tosi 1 , Dasiel Obregón 1,2 , Kari E. Dunfield 1* and
James J. Germida 3*
1
School of Environmental Sciences, University of Guelph, Guelph, ON, Canada, 2 Centre for Nuclear Energy in Agriculture,
University of Sāo Paulo, Piracicaba, Brazil, 3 Department of Soil Science, University of Saskatchewan, Saskatoon, SK, Canada
Global population growth poses a threat to food security in an era of increased

ecosystem degradation, climate change, soil erosion, and biodiversity loss. In this
context, harnessing naturally-occurring processes such as those provided by soil and
Edited by: plant-associated microorganisms presents a promising strategy to reduce dependency
Maryke T. Labuschagne, on agrochemicals. Biofertilizers are living microbes that enhance plant nutrition by either
University of the Free State,
by mobilizing or increasing nutrient availability in soils. Various microbial taxa including
South Africa
beneficial bacteria and fungi are currently used as biofertilizers, as they successfully
Reviewed by:
Tahira Fatima, colonize the rhizosphere, rhizoplane or root interior. Despite their great potential to
Purdue University, United States improve soil fertility, biofertilizers have yet to replace conventional chemical fertilizers in
Senthilkumar Murugaiyan,
Tamil Nadu Agricultural commercial agriculture. In the last 10 years, multi-omics studies have made a significant
University, India step forward in understanding the drivers, roles, processes, and mechanisms in the
*Correspondence: plant microbiome. However, translating this knowledge on microbiome functions in order
Kari E. Dunfield
to capitalize on plant nutrition in agroecosystems still remains a challenge. Here, we
dunfield@uoguelph.ca
James J. Germida address the key factors limiting successful field applications of biofertilizers and suggest
jim.germida@usask.ca potential solutions based on emerging strategies for product development. Finally, we
discuss the importance of biosafety guidelines and propose new avenues of research for
Specialty section:
This article was submitted to biofertilizer development.
Crop Biology and Sustainability,
Keywords: plant growth promotion, microbiome, plant nutrition, bioprospecting, soil health, sustainable
a section of the journal
agriculture, inoculation, bioformulation
Frontiers in Sustainable Food Systems
Received: 15 September 2020

Accepted: 18 January 2021
Published: 19 February 2021
INTRODUCTION
Citation: Soil and plant-associated microbes play a key role in ecosystem functioning by carrying
Mitter EK, Tosi M, Obregón D, out numerous biogeochemical cycles and organic matter degradation (Paul, 2015). For this
Dunfield KE and Germida JJ (2021)
reason, biofertilizers (i.e., microbial-based fertilizers) are considered to be crucial components
Rethinking Crop Nutrition in Times of
Modern Microbiology: Innovative
of sustainable agriculture, with long lasting effects on soil fertility (Bargaz et al., 2018; Singh
Biofertilizer Technologies. et al., 2019). The term biofertilizer can be defined as formulations comprised of living microbial
Front. Sustain. Food Syst. 5:606815. cells, either a single strain or multiple strains (mixed or consortium), that promote plant
doi: 10.3389/fsufs.2021.606815 growth by increasing nutrient availability and acquisition (Riaz et al., 2020). Nevertheless, the
Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2021 | Volume 5 | Article 606815
Mitter et al. Innovative Biofertilizer Technologies
term itself has evolved over the last 30 years receiving many carbon, and oxygen (Howarth, 2009). For example, N is an
interpretations (El-Ghamry et al., 2018; Macik et al., 2020). essential component of chlorophyll, amino acids, nucleic acids,
As stated by Macik et al. (2020), the greatest misconception and the energy transfer molecule adenosine triphosphate (ATP)
occurs when including microbial inoculants with other beneficial (Werner and Newton, 2005). One important source of N in
applications (e.g., biopesticides and phytostimulators) as soils is organic N which requires microbial mineralization to
biofertilizers. Likewise, plant growth-promoting bacteria or be converted to plant available inorganic N, a combination
rhizobacteria (PGPB/PGPR) and biofertilizers should not be of ammonification and nitrification (Paul, 2015). However,
considered an interchangeable term, since not all PGPB/PGPR the major N reservoir is in the atmosphere as N2 , which
are biofertilizers (Riaz et al., 2020). Nonetheless, it is worth is not directly used by plants and only becomes available
mentioning that biofertilizers can also provide other direct and through Biological N2 -fixation (BNF) (Figure 1). This is an
indirect benefits for plant growth, such as phytostimulation, energy-intensive process by which the enzyme nitrogenase
abiotic stress tolerance and biocontrol (Ferreira et al., 2019; Liu converts atmospheric N2 to ammonia (NH3 ), which is readily
et al., 2020; Shirmohammadi et al., 2020). available for assimilation by plants and microbes (Dakora et al.,
The commercial history of biofertilizers dates back to 1895 2008). Nitrogenases can be found in a small and diverse
using “Nitragin” by Nobbe and Hiltner with a laboratory group of microorganisms called diazotrophs (N2 -fixing), which
culture of Rhizobium sp. (Singh et al., 2019). In the late includes symbiotic bacteria, and free-living bacteria and archaea
1950s, several studies with arbuscular mycorrhizal fungi (Moreira-Coello et al., 2019). In agriculture, the most studied
inoculants reported positive plant growth promotion (PGP) symbiotic N2 -fixing organisms are bacteria known as rhizobia,
effects through phosphorus (P) uptake (Koide and Mosse, comprised mostly of the family Rhizobiaceae [i.e., Rhizobium,
2004). However, despite their numerous advantages and Bradyrhizobium, Sinorhizobium, Azorhizobium, Mesorhizobium,
low cost, the commercialization of biofertilizers is not and Sinorhizobium (Ensifer)] (Shamseldin et al., 2017). Rhizobia
widespread. The reasons limiting their use are mostly can establish symbiotic relationships with legumes (family
related to inconsistent responses over different soils, Fabaceae) by forming nodules on their roots or stems (Masson-
crops and environmental conditions, along with practical Boivin and Sachs, 2018). These nodules provide an advantage
aspects related to mass production, shelf-life, appropriate for N2 -fixation in which nitrogenases are protected in bacteroids
recommendations and ease of use for farmers (Debnath et al., from atmospheric O2 . The oxygen concentration is an important
2019). factor determining the amount of N that is fixed, since oxygen
In the last 10 years, multi-omics technologies enhanced our is a negative regulator of nif gene expression and inhibits
understanding of the complexity of microbiomes, as they allowed nitrogenase activity (Glick, 2015). Several rhizobia, such as
us to better characterize the structure and function of microbial Rhizobium, Sinorhizobium (Ensifer), and Bradyrhizobium, are
communities (Kaul et al., 2016). These novel approaches are commonly used as biofertilizers in agriculture (Carareto Alves
increasingly applied to describe soil microbial communities and et al., 2014). Plants can acquire a significant proportion of
their influence on plant nutrient acquisition and other PGP traits their N requirement through associations with the diazotrophs
(Saad et al., 2020; Tosi et al., 2020a,b). However, they have yet to (Dakora et al., 2008). For example, N2 -fixation could supply
be successfully applied in the development of novel and improved ∼20–25% of total N requirement in rice, ∼30–50% in wheat
biofertilizer technologies (Qiu et al., 2019). and up to 70% in sugarcane (Hurek et al., 2002; Gupta
In this review, we focus on the direct mechanisms and Paterson, 2006; Santi et al., 2013). Yet, the amount
by which microorganisms enhance the availability and of N provided by BNF will vary depending on the plant
acquisition of essential plant nutrients. Subsequently, we species and environmental factors, which will ultimately
assess the current challenges and constraints faced by the determine a successful colonization (Parnell et al., 2016), as
implementation of biofertilizers in agriculture, and we explained below.
discuss emerging strategies for biofertilizer development In contrast to symbiotic N2 -fixing bacteria, several
(e.g., bioprospecting and formulations). Finally, we address heterotrophic free-living diazotrophic microorganisms such
the potential risks that biofertilizers pose to human and as Azotobacter sp., Azospirillum sp., and cyanobacteria
environmental health, and conclude by highlighting can fix atmospheric N2 in the rhizosphere and bulk soil.
current knowledge gaps and identifying priorities for Free-living diazotrophs are particularly important for N
future research. acquisition in non-legume crops. For example, increased
crop yields were observed in cereals (e.g., wheat, rice, and
corn) and a variety of other crops such as sunflower, carrot,
AN OVERVIEW OF BIOFERTILIZERS: KEY oak, sugar beet, sugarcane, tomato, eggplant, pepper, and
MECHANISMS OF NUTRIENT cotton (Garcha and Maan, 2017). Azospirillum species can
ACQUISITION carry out several PGP functions but are also the most
well known free-living diazotrophs, shown to enhance N
Nitrogen: N2 -Fixation availability and acquisition in more than 113 plant species
Nitrogen (N) is an essential element for life and it is the fourth (Bashan and De-Bashan, 2010; Pereg et al., 2016; Zeffa et al.,
most abundant element in all living biomass after hydrogen, 2019).
FIGURE 1 | Key microbially-mediated nutrient transformation/acquisition pathways associated with biofertilizers. Full arrows represent microbial transformations
whereas dashed arrows represent mobilization/movement of nutrients. Created with BioRender (https://biorender.com/).
Phosphorus: Solubilization and solubilization and mineralization (Alori et al., 2017) (Figure 1).
Mineralization Phosphate-solubilizing microbes (PSM) solubilize inorganic P
Phosphorus is one of the most important plant nutrients (e.g., tricalcium phosphate, hydroxyapatite, and rock phosphate)
that directly or indirectly affects all biological processes. For via the production and release of different compounds. One
example, P is key in all major plant metabolic processes such as mechanism consists in the excretion of organic acids, hydroxyl
photosynthesis, energy transfer, signal transduction, biosynthesis ions and CO2 , which dissolve the insoluble phosphates directly
of molecules, and respiration. A considerable amount of P is by lowering the soil pH, then leading to ion exchange of PO4 2−
present in soils, in both inorganic and organic forms, but its by acid ions (Wei et al., 2018). Microbes can also release chelating
availability is one of the main factors limiting plant growth compounds that capture and mobilize cations from different
in many ecosystems worldwide (Raghothama, 2015). This is insoluble phosphates such as Ca+2 , Al+3 , and Fe+3 , resulting
because most soil P is in an occluded or insoluble form, and in the release of associated soluble phosphates (Riaz et al.,
unavailable for plants, which can uptake P from the soil solution 2020). By increasing P bioavailability, PSM reduce the need for
as orthophosphate ions H2 PO− 2− (Soumare et al., mineral P fertilizer inputs, which in excess can lead to negative
4 and HPO4
2020). The concentration of soluble phosphates (PO4 3− ) in environmental impacts such as eutrophication of fresh-water
the soil solution is generally low, around 0.001–0.4 mg P/L in bodies. The most studied P solubilizers belong to the genera
unfertilized soils, which is equivalent to 0.001–0.01% of total- Pseudomonas, Bacillus, Rhizobium, Enterobacter, Penicillium, and
P (Weihrauch and Opp, 2018). In addition, it is estimated that Aspergillus (De Freitas et al., 1997; Anand et al., 2016).
∼80% of the P applied via fertilization gets quickly fixed into Another important process by which soil microorganisms
stable forms in the soil, unavailable for plants (Pradhan et al., can increase P bioavailability is by the mineralization of organic
2017). phosphate compounds (e.g., inositol hexaphosphate and phytate)
Soil microbes are capable of converting insoluble soil P (Alori et al., 2017). This process is mediated by phosphatases (e.g.,
into plant available form(s) through various mechanisms of phosphodiesterases and phosphomonoesterases) and phytases
that help release phosphate from organic P compounds, which to be oxidized to SO2− 4 in order to become available to plants
can then be taken up by plants (Pradhan et al., 2017). (Scherer, 2009).
The application of S-oxidizing microbes can help by both
optimizing S fertilization and minimizing environmental risks
Potassium: Solubilization caused by S leaching (Figure 1). Sulfur-oxidizing bacteria can
Potassium (K) is a vital plant macronutrient and a major
use S0 as an energy source, releasing plant-available sulfate.
inorganic cation in the plant cytoplasm, essential for cell
Hence, their inoculation together with S0 fertilizers can speed
constitution and functioning, implicated in photosynthesis,
up its conversion to sulfates, potentially leading to higher crop
protein synthesis, and many other primary metabolic functions.
yields (Pujar et al., 2014). Sulfur-oxidizing biofertilizers have been
Potassium is also the second most abundant nutrient in soil
recommended for grain crops (e.g., oilseed species, oats) and
after N, and one of the most abundant elements on Earth.
horticultural crops (e.g., onion, cauliflower, ginger, garlic) (Santra
However, ∼98% of soil K is present in a non-exchangeable form,
et al., 2015). Sulfur oxidation in soil is carried out by a variety of
trapped within crystal structures of the minerals feldspar and
archaea and bacteria such as the genera Xanthobacter, Alcaligenes,
mica (e.g., muscovite, biotite). Another 1–2% is adsorbed onto
Bacillus, Pseudomonas, Streptomyces, and Thiobacillus, as well as
clay particles and organic matter, while only 0.1–0.2% is in the soil
fungi including Fusarium, Aspergillus, and Penicillium (Grayston
solution and directly available for plant uptake (Srivastava et al.,
et al., 1986; Germida and Janzen, 1993; Macik et al., 2020).
2019). Currently, Canada is the world’s largest potash producer
with approximately one-third of the world potash reserves
located in southern Saskatchewan (Broughton, 2019). However, Micronutrients: Chelation and
especially in the Southern Hemisphere, several countries with
little or no potash production are highly-dependent on the
Solubilization
Micronutrients such as iron (Fe), zinc (Zn), cooper (Cu),
import of fertilizers and need alternatives to increase soil
manganese (Mn), boron (B), molybdenum (Mo), chlorine (Cl),
K availability.
nickel (Ni), cobalt (Co), and silicon (Si), are essential for plants
Microorganisms can increase K availability via solubilization,
(Shukla et al., 2018). These are essential for plant development
a process that plays a key role in the K cycle by making K
as they are involved in critical enzymatic reactions including
available to plants (Sattar et al., 2019; Macik et al., 2020)
photosynthesis, respiration, water oxidation, and oxidative stress
(Figure 1). Similar to P, the most well-known mechanism of
protection (Castro et al., 2018). In fact, several studies revealed
microbial K solubilization involves the synthesis and discharge
that micronutrient deficiencies hamper crop production in many
of organic acids (i.e., tartaric, citric, oxalic, gluconic, lactic,
areas of the world; especially in alkaline soils with low organic
and malic acid) (Sattar et al., 2019). These organic acids
matter content (Rashid and Ryan, 2004).
lead to the acidification of the surrounding environment
One of the most studied mechanisms for increasing
and therefore the release (acidolysis) of K+ from minerals
micronutrient availability is iron sequestration via siderophores
(Sattar et al., 2019). Other important K release mechanisms
(Rroço et al., 2003). Under Fe-limiting conditions, these low
include chelation, and exchange reactions involving organic
molecular weight chelating compounds scavenge Fe3+ (the most
acids (Sharma et al., 2016). Several groups of soil bacteria
common form in soils) from the mineral phases, forming
(e.g., Bacillus, Rhizobium, Acidithiobacillus, Paenibacillus,
soluble Fe3+ complexes that are accessible for plant uptake
Pseudomonas, and Burkholderia) and fungi (Aspergillus,
(Figure 1). In general, plant species such as barley, rye,
Cladosporium, Macrophomina, Sclerotinia, Trichoderma,
and wheat, can produce high concentrations of siderophores
Glomus, and Penicillium) can solubilize K minerals (Kour et al.,
and, thus are more resistant to iron deficiency (Ahmed
2020).
and Holmström, 2014). However, other crops (e.g., maize,
sorghum, and rice) with lower siderophore production can
Sulfur: Oxidation benefit from siderophore-producing microorganisms. There are
Sulfur (S) is an essential nutrient for plant growth, implicated in three main classes of fungal siderophores (i.e., rhodotorulic
the conformation of biomolecules such as proteins, glutathione, acid, ferrichromes, and fusarinines) and four classes of
chloroplast membrane lipids, coenzymes, and vitamins. Most S bacterial siderophores (i.e., phenol-catecholates, hydroxamates,
in soils (∼95%) is in an organic form (C-bonded S or sulfate carboxylate, and pyoverdines) (Crowley, 2006). In agricultural
esters), while inorganic forms are less common (5–10%). The plants, siderophore production by Pseudomonas fluorescens was
most common form of inorganic S is sulfate (SO4 2− ), which is shown to play a role in Fe nutrition and PGP in tomato (Nagata,
readily available for plant uptake and is present either dissolved 2017), pea (Lurthy et al., 2020) and sorghum (Abbaszadeh-
in the soil solution or adsorbed to soil particles (Scherer, 2009). Dahaji et al., 2020) under Fe limiting conditions. Apart from Fe,
In the last decades, S deficiency in agricultural soils increased siderophores are also known to bind other metals (e.g., Al3+ ,
on a worldwide scale, likely as a consequence of the decline Cd2+ , Co2+ , Cu2+ , Hg2+ , Mn2+ , Ni2+ , and Pb2+ ) (Saha et al.,
in atmospheric deposition of S due to the reductions in SO2 2013) (Figure 1).
emissions and the use of low-S fertilizers (Ercoli et al., 2012). Zinc deficiency is the most important micronutrient problem
Consequently, S fertilizers have received increasing attention, in crops, causing root necrosis, reduction of biomass and yield,
with elemental S (S0 ) as the most common form of S fertilizer. and high plant mortality (Caldelas and Weiss, 2017). Also, it
Elemental S constitutes a highly concentrated form of S but needs is estimated that more than 84% of total soil Zn occurs as
structurally lattice bound [e.g., zincite (ZnO) and zinc sulfide be discussed below, their reliability is still limited (Hart et al.,
(ZnS)], while only 1% is in water soluble form and available 2018).
for plant uptake (Sharma et al., 2013; Prasad et al., 2016). Besides AMF, efforts are being made to use other endophytic
Consequently, Zn is now integrated into chemical fertilizers (i.e., fungi to improve crop nutrient acquisition and growth (Murphy
applied along with NPK) for most crops in several countries et al., 2018). Among these, root-colonizing dark septate
(Prasad et al., 2016). However, most of this water-soluble Zn (96– endophytes (DSE) are a diverse group, mostly belonging to the
99%) is rapidly converted to insoluble forms, and only 1–4% of phylum Ascomycota, which could potentially provide benefits
the total applied Zn can be used by plants (Kushwaha et al., 2020). ranging from nutrient acquisition to disease and abiotic stress
A solution to this problem is the application of Zn-solubilizing tolerance (He et al., 2019a; Spagnoletti and Giacometti, 2020).
microbes (ZSM) as biofertilizers to increase Zn availability in soils These DSE have been found in over 600 plant species, some of
where this micronutrient is present in high concentrations but them non-mycorrhizal, and several studies show their potential
insoluble forms (Sammauria et al., 2020) (Figure 1). Similarly to to enhance N uptake in crops such as rice and tomato (Mandyam
other solubilizers, these ZSM are capable of solubilizing Zn by and Jumpponen, 2005; Mahmoud and Narisawa, 2013; Vergara
acidification, chelation, and chemical transformation (Kushwaha et al., 2018). Their effect on P acquisition has been less studied,
et al., 2020; Macik et al., 2020). but evidence suggests they could also assist on the solubilization
In 2013, Si was classified as a beneficial nutrient by of Ca, Al, and Fe phosphates (Spagnoletti et al., 2017).
the Association of American Plant Food Control Officials
(AAPFCO), due to the increasing knowledge of Si effects on
plant growth and protection (Heckman, 2013). In soils, most Si CURRENT CHALLENGES LIMITING
is in recalcitrant silicate minerals (i.e., aluminum silicates and BIOFERTILIZER APPLICATIONS
quartz) and only a much smaller fraction is available for plants
(Greger et al., 2018). The plant-available Si is in the form of There are several key steps to be overcome by introduced
monosilicic acid (H4 SiO4 ), present both in the soil solution and microbe/s before achieving the desired effects in plant
adsorbed phases (Fe and Al oxides/hydroxides) (Tubaña and growth and fitness: survival, establishment, colonization,
Heckman, 2015). Silicate-solubilizing bacteria occurring in soils and interaction with the plant (e.g., parasitic/symbiotic behavior,
and rhizosphere act by solubilizing silicates (Figure 1). The most PGP performance). This is particularly concerning in the
studied species are from the genera Burkholderia, Aeromonas, lab-to-field transition, where it is common for a microbial
Rhizobium, Enterobacter, and Bacillus (Santi and Goenadi, 2017; strain with good performance in vitro to perform poorly in
Lee et al., 2019). greenhouse and/or field trials (Parnell et al., 2016; Hart et al.,
2018; Keswani et al., 2019). The inoculation outcome is especially
hard to predict because we generally consider and control for
a limited number of variables, usually not taking into account
Nutrient Mobilization and the Role of their intricate interactions (Moutia et al., 2010; Sasaki et al.,
Root-Associated Fungi 2010; Busby et al., 2017). Here, we summarize the main factors
The most studied case among root-associated fungi are associated with inoculation success by classifying them into
arbuscular mycorrhizal fungi (AMF), obligate symbionts plant-related, edaphic/environmental, and inoculant-related
from the phylum Glomeromycota which can form symbiotic (e.g., additives, concentration, viability) (Malusà et al., 2016)
relationships with ∼80% of land plant species, including (Table 1), as well as the practical aspects that currently limit the
agricultural crops (Berruti et al., 2016). Among other benefits, applicability of biofertilizers in agriculture.
AMF can enhance the uptake of mineral nutrients (i.e., P, N,
S, Cu, and Zn) and water by their host plants (Bücking and Edaphic and Environmental Conditions
Kafle, 2015) in exchange for carbon sources (Hodge and Fitter, Edaphic and environmental conditions are two major factors
2010; Veresoglou et al., 2012). The extraradical AMF mycelium behind the variability and low reproducibility of biofertilizers
increases the volume of soil explored not only by reaching far in field trials (Hoeksema et al., 2010; Da Costa et al., 2014;
beyond the rhizosphere but also by penetrating smaller soil Schütz et al., 2018). Initial steps of biofertilizer testing are
pores (Berruti et al., 2016). This is particularly important for carried out in aseptic controlled conditions, which allow for an
the acquisition of less mobile nutrients such as P and, in fact, unbiased characterization of the microorganism under study.
AMF are well-known for their ability to enhance P acquisition, Scaling up to growth chamber or greenhouse trials, and especially
especially in P-deficient soils (Kumar et al., 2018) (Figure 1). to field conditions, increases the number of uncontrolled biotic
Arbuscular mycorrhizae were also shown to facilitate N uptake, and abiotic factors that can interfere with inoculation success
mostly in the form of ammonium (NH+ 4 ) (Hodge and Fitter, (Nkebiwe et al., 2016; Bacilio et al., 2017). Among the biotic
2010; Veresoglou et al., 2012). Over the last decades, several factors that can affect the outcome of inoculation, the most
companies manufactured and commercialized AMF inoculants discussed is the presence of competitors, predators, or other
and the global mycorrhiza-based biofertilizer market is projected antagonists within the resident microbiome (i.e., indigenous and
to be worth 621.6 million US dollars by 2025. These products previously introduced microorganisms) (Biró et al., 2000; Vargas
are especially being encouraged in countries of the Asia Pacific et al., 2000; Ortas, 2003). Abiotic factors, either climatic or
region such as India and China (ReportLinker, 2020) but, as will edaphic, can also influence the effectiveness of biofertilization
TABLE 1 | Challenges associated with biofertilizer success and potential solutions relying on novel technologies.
Challenges Potential solution(s)
Edaphic and Biotic Negative interactions with the resident microbiome (e.g., Personalized biofertilizers for a specific farm (e.g.,
environmental competition, predation, and antagonism). particular soil, crop and management).
Abiotic High variability in soil physicochemical properties (e.g., Biofertilizers based on optimal range of
nutrient levels, pH, organic matter content, moisture, performance.
temperature, salinity).
Agricultural practices Interaction with other agricultural practices (e.g., organic
amendments, fertilizers, pesticides, tillage, crop
diversification strategies).
Plant-related Plant genotype and Different outcomes depending on plant genotype due to Isolated compounds or “prebiotics” (e.g.,
physiological status different degrees of specificity or indirect selection via benzoxazinoids, coumarins, triterpenes) to attract or
plant rhizodeposition and root architecture. favor microbe/s of interest.
Variability in different plant growth stages and overall Genotype-specific inoculum (e.g., compatible
physiological status. microorganisms, pre-adapted microbiome).
Optimized application timing.
Inoculant-related Genetic and Microbes with poor ecologically relevant traits affecting Pre-adapted microorganisms (e.g., isolated locally),
physiological traits their establishment, colonization, persistence and isolation and screening focused on both PGP and
tolerance to abiotic stresses (e.g., osmotic and ecological traits.
temperature). Engineered microbial communities (e.g., SynComs)
or whole microbiomes.
Mixed inoculants with functional redundancy but a
wide range of environmental adaptation.
Biofilm-forming microorganisms.
Formulations Insufficient physical and chemical protection to maintain Processes based on different methods such as
cell viability and prevent desiccation/contamination. alginate microencapsulation and fluidized bed dryer
(FBD).
Practical aspects Costs Economic feasibility at a commercial scale Resource inputs from public and private sectors
(bioprospecting, testing, scaling up, storage, and encouraged by regulatory agencies and policy
application). makers (e.g., incentives, promotion, and
awareness).
Farmer accessibility Products with limited versatility, reproducibility, shelf-life,
practicality (handling and application), adaptability to
different agricultural practices.
Insufficient collaboration and communication between
researchers, industry, and farmers.
Regulations Lack of standardized and universal testing protocols and
evaluation guidelines.
Intellectual property Disregard or negligence to protect intellectual property
(patent development) and technology transfer.
on crop nutrient use efficiency and yield. According to a meta- effects of microbial inoculation with chemical fertilizers (Ozturk
analysis by Schütz et al. (2018), biofertilizers generally perform et al., 2003; Jansa et al., 2009; Da Costa et al., 2014), organic
better under drier climatic conditions, higher soil P levels amendments (Manandhar et al., 2017; Ulzen et al., 2019),
(especially for N2 -fixers) and, exclusively for AMF, lower soil pesticides (Gaind et al., 2007; Jin et al., 2013b), and tillage
organic matter content and neutral pH. Yet, higher growth (Miller et al., 1995; Mulas et al., 2015). It is also expected
and yield responses to biofertilization are usually observed that crop diversification practices (e.g., rotations, cover crops)
under low nutrient availability (Ozturk et al., 2003; Da Costa could modulate biofertilization efficiency by modifying resident
et al., 2014), as the plant can fully benefit from the interaction microbial communities (Maiti et al., 2011; Buysens et al.,
with the introduced microbe. The negative relationship between 2016).
biofertilization success and soil nutrient content has been widely
studied both for AMF colonization with soil P (Kaeppler Plant-Related Factors
et al., 2000; Jansa et al., 2009), and rhizobia nodulation with Biofertilization can lead to different outcomes depending on the
soil N (Glyan’ko et al., 2009; Thilakarathna and Raizada, selected crop species or genotype. Although some studies are
2017). beginning to identify genetic markers (e.g., quantitative trait loci
Some edaphic properties can also be highly susceptible to or QTLs) associated with this differential response (Kaeppler
agricultural practices, therefore generating additional variability et al., 2000; Remans et al., 2008), the plant factors behind them
in inoculation success. So far, evidence has shown interacting are not yet clearly understood. In general terms, it is known that
plants can directly and indirectly alter the rhizosphere habitat or, instead, pursuit broad-spectrum versatile products? (Parnell
through rhizodeposits and changes in the root architecture et al., 2016; Bell et al., 2019; Tosi et al., 2020a). In the
(Somers et al., 2004; Saleem et al., 2018). Among their many latter, the outcome would imply either utilizing versatile
rhizodeposits, plant roots secrete signaling molecules such as microbes or formulating mixed inoculants that expand the
secondary metabolites (e.g., flavonoids, hormones, antibiotics), ecological adaptation range (i.e., functionally redundant strains
some of which are important in the recognition and interaction that encompass a wider range of environmental adaptation).
with PGP microbes (Bais et al., 2004). The degree of specificity In spite of the challenges arising from the interaction and
of this signaling process can be high for certain symbioses possible interference among members of a mixed inoculant,
such as rhizobia-legumes, where the compatibility between which will differ on each particular scenario (Xavier and
microbes and host plants is crucial to establish a successful Germida, 2003; Remans et al., 2008; Ballesteros-Almanza et al.,
colonization (Hirsch et al., 2003; Thilakarathna and Raizada, 2010), they bear great potential for overcoming the issues of
2017). In the case of arbuscular mycorrhiza, host specificity environmental adaptability.
might not be as critical (Koyama et al., 2017) but colonization Besides the identity of the inoculated microbe, biofertilizer
and PGP can still be affected by the plant genotype (Yao concentration, formulation, and delivery practices will also
et al., 2001; Linderman and Davis, 2004; Hoeksema et al., determine how tolerant and protected inoculated microbes will
2010). Studies have explained these different levels of AMF- be from environmental constraints. The inoculant formulation
host plant compatibility through differences in root architecture should be able to support microbial growth, while protecting
(Declerck et al., 1995), aerial architecture (Liu et al., 2000), an amount of viable cells high enough for an effective
and P utilization and uptake efficiency (Kaeppler et al., 2000; response in the plant (Herrmann and Lesueur, 2013; Bashan
Yao et al., 2001). Significant specificity between microbe and et al., 2014). Additional challenges associated with scaling
plant genotype was also observed for endophytes (Muñoz-Rojas up and commercializing a microbial product include, but
and Caballero-Mellado, 2003; Yoon et al., 2016; Vujanovic and are not limited to, a risk of genetic and physiological
Germida, 2017) and free-living PGPR such as Azospirillum spp. changes in the strain, viability loss (particularly by desiccation)
(Sasaki et al., 2010; Vargas et al., 2012), Pseudomonas sp. (Digat and contamination (Parnell et al., 2016; Glick, 2020; Greffe
et al., 1990; Safronova et al., 2006), and Azotobacter sp. (Mezei and Michiels, 2020). With the expansion in the biofertilizer
et al., 1997; Anbi et al., 2020). Considering that most plant industry, novel and more sophisticated formulations have been
breeding programs do not address plant-microbe interactions, developed, including a variety of solid, slurry, and liquid
plant genotype-induced variability in biofertilization outcomes carriers, as well as a wide array of additives (e.g., nutrients,
remains a major concern. Furthermore, genotype effects are not stimulants, preservatives) to enhance the physical properties
isolated, but modulated by plant age and physiological status of the inoculant (e.g., adhesives, surfactants) (Bashan et al.,
(Dennis et al., 2010), which will be ultimately determined by 2014, 2016; Preininger et al., 2018). These additives allow
surrounding environmental conditions and time of inoculation. microbes to withstand the fluctuating and suboptimal conditions
during distribution, storage, and application (Parnell et al.,
Inoculant-Related Factors 2016) (further discussed in section New Formulations and
The selected microbial genotype not only determines its Delivery Methods). Even though these carriers and additives
PGP functions, but also its compatibility with the plant seem to be a secondary aspect of biofertilizer development,
host genotype (Linderman and Davis, 2004; Vargas et al., they can be critical for obtaining successful results (Gomez
2012; Ehinger et al., 2014). Furthermore, microbial traits et al., 1997; Herrmann and Lesueur, 2013; Lee et al.,
also determine key aspects of inoculation such as survival 2016).
(before and after application), establishment, colonization, and Similarly, delivery methods (e.g., on seed or into soil),
persistence. Generally, inoculant development focuses on genetic and application timing and frequency can be critical for
and PGP traits, with little or no attention to ecological traits, inoculation success (Parnell et al., 2016). For example, in a
which will ultimately determine inoculation success under field rhizobia inoculation trial on Pisum sativa, soil applications
conditions (Hart et al., 2018; Kaminsky et al., 2019). For of a granular inoculant resulted in higher PGP than seed
example, strains adapted to specific environmental conditions applications of a liquid formulation (Clayton et al., 2004).
can be selected by focusing on specific traits such as osmotic Foliar and flower applications were also being considered as
tolerance (García et al., 2017) or psychrotolerance (Rawat a safer and more effective delivery strategy for endophytic or
et al., 2019). Another approach consists in the isolation of phyllosphere microorganisms (Mitter et al., 2013; Preininger
native strains, which were shown to improve biofertilization et al., 2018). Application timing and frequency should be
performance (Melchiorre et al., 2011; Ahmed et al., 2013; also taken into consideration in relation to plant growth
Maltz and Treseder, 2015). Yet, there seems to be a trade- stages (Bashan, 1986; Fallik et al., 1988; Linderman and
off between establishment and survival traits and PGP traits, Davis, 2004), as well as other agricultural practices such as
posing a challenge at each of the different stages of inoculant fertilization (Pii et al., 2019) and transplant (Sohn et al., 2003).
development (Parnell et al., 2016; Kaminsky et al., 2019). This The time elapsed between application and establishment is
trade-off, together with the high specificity of microbial strains to critical, as it will determine the survival of the microbe to
both environment and host genotype, leads to a crucial question: environmental constraints before it can provide any benefits to
should we aim for more specific and targeted biofertilizers the plant.
Practical Aspects New Culture-Dependent Methods

We have discussed major technical limitations that can markedly Since Antony Van Leeuwenhoek’s discovery of microorganisms
affect biofertilizer efficiency, but there is also a set of practical in the 1670s, isolation and cultivation of microbes are the major
aspects that cannot be overlooked in biofertilizer development. pillars of microbiology (Oren and Garrity, 2014). Since then, the
One of these concerns is the accessibility and convenience best practices for culturing new organisms have been developed
of inoculants for both farmers and manufacturers, especially and published in guides such as the Bergey’s Manual of Systematic
in comparison with chemical fertilizers. Some key factors Bacteriology (Boone et al., 2001). However, in the last 20 years,
related to biofertilizer accessibility are: cost/benefit relationship, the use of diffusion chambers (Kaeberlein, 2002; Bollmann et al.,
versatility, robustness and reproducibility, shelf-life and storage 2007) and isolation chips (Ichip) (Nichols et al., 2010), that mimic
requirements, ease of use (handling and application), adaptability natural environments, increased the number of cultured colonies
to agricultural practices and machinery, and biosafety (Bashan and marked a rebirth of culture dependent techniques. Most
et al., 2014; Parnell et al., 2016; Bell et al., 2019). Novel products recently, studies by Lagier et al. (2015, 2016) used “culturomics”
should be accompanied by a better outreach in order to inform to cultivate previously uncultured members of the human
farmers on the benefits of biofertilizers, particularly in the longer gut microbiota. Culturomics uses multiple culture conditions,
term, and to facilitate and promote their application (Parnell MALDI-TOF mass spectrometry and 16S rRNA sequencing for
et al., 2016; Martínez-Hidalgo et al., 2018). A less discussed the identification of bacterial species (Lagier et al., 2018). The
issue are intellectual property rights and patent development, main objective of this technique is to suppress the culture of fast-
which can be a valuable tool to transfer technology between the growing and highly abundant species and to promote the growth
academic and industrial sector, but could also put at risk the free of fastidious and/or less abundant microorganisms (Lagier et al.,
exchange of ideas and materials among researchers (Glick, 2020). 2015).
Product commercialization also requires proper regulations Despite its success on the human microbiota, multiple
(Sessitsch et al., 2019) with standardized and universal testing combinations in culturomics (i.e., various growth media,
protocols and risk evaluation guidelines (Vílchez et al., 2016; culturing conditions, atmospheres, and times of incubation)
Timmusk et al., 2017). Finally, the research and development have yet to be extended and developed for the soil and plant-
sector are still in need of standardized protocols to evaluate associated microbiome. In order to minimize these challenges,
inoculation success (Hart et al., 2018; Martínez-Hidalgo et al., Sarhan et al. (2019) suggested a “plant-tailored culturomic
2018; Kaminsky et al., 2019) and to monitor microbes once technique” that combines culturomics with plant-based media.
applied in the field (Schütz et al., 2018; Compant et al., 2019). According to these authors, most studies continue to use
general media containing nutrients of animal origin (e.g.,
nutrient agar, R2A, and LB) to isolate plant associated microbes,
NEW APPROACHES IN BIOFERTILIZER whereas plant materials or dehydrated juices powders should be
DEVELOPMENT used instead. In fact, P-solubilizing Bacillus circulans and N2 -
fixing Azospirillum brasilense have been successfully grown on
In recent years, product development strategies have shifted from plant-only-based culture media (Youssef et al., 2016; Mourad
single-strain to microbial consortia inoculation. These strategies et al., 2018). In addition, online platforms such as KOMODO
are based on a greater chance of at least one strain escaping (Known Media Database, http://komodo.modelseed.org) that
competitive exclusion, and thus ensuring inoculant survival includes >18,000 strain–media combinations and >3,300 media
and function (Rivett et al., 2018; Tosi et al., 2020a). Microbial variants/compound concentrations can be used as a guide for
consortia can consist of two or more strains that are either developing suitable lab media for growing microorganisms
closely (Kyei-Boahen et al., 2005; Jin et al., 2013a) or distantly (Oberhardt et al., 2015). Therefore, new culturing methods to
(Ramírez-López et al., 2019; El Maaloum et al., 2020) related that discover novel isolates with biotechnological applications are key
provide an overall additive or synergistic biofertilization effect. for biofertilizer development. Unfortunately, newly culturable
One of the most common applications is the co-inoculation of microorganisms (e.g., slow growers) may still be less reliable and
rhizobia and AMF on legumes, as a number of studies report cost-effective for mass production with our current technology.
a synergistic effect on plant growth promotion (Xavier and
Germida, 2003; Ashrafi et al., 2014; Kamaei et al., 2019). Yet, How to Artificially Select Microbiomes?
examples in the literature also show negative effects of AMF There are two main approaches to artificially select microbiomes:
on nodule development or non-significant effects on crop yield “top-down,” which modifies an existing microbiome, and
(Antunes et al., 2006; Menéndez and Paço, 2020). Despite the “bottom-up,” which starts from individual microorganisms
promising beneficial effects of developing biofertilizers consisting to build artificial or engineered microbiomes (e.g., synthetic
of microbial consortia, it is unknown how these inoculants communities or SynComs). In the “top-down” approach, selected
would establish across a range of agricultural field settings environmental variables (e.g., pH, temperature, redox potential)
(Finkel et al., 2017). Moreover, even if inoculated microbes are used to manipulate an existing microbiome, through
colonize their new environment initially, their persistence over ecological selection, to perform desired functions (Lawson et al.,
time is not guaranteed. Here, we discuss new approaches 2019). Although this approach is widely used for bioremediation
to develop suitable bioinoculants at commercial scale from (Atashgahi et al., 2018) and wastewater treatment (Demarche
screening potential candidate microorganisms, designing the et al., 2012), it has the disadvantage of working with a
inoculant and optimizing formulations. complex community. In contrast, “bottom-up” approaches offer
the advantage of simplifying these interactions by building et al., 2015; Lebeis et al., 2015). In studies by Castrillo et al. (2017),
artificial communities from pre-selected individual organisms SynComs were used to investigate links between Arabidopsis
(Raaijmakers, 2015). phosphate starvation response, immune system function, and
Given the high complexity of molecular-scale microbiome root microbiome assembly. In agricultural crops, Armanhi et al.
processes, most of the challenges in designing microbial (2018) designed a SynCom comprised of naturally occurring
inoculants is to identify key beneficial microorganisms (e.g., bacterial groups in the sugarcane microbiome and tested using
Azotobacter, Rhizobium, Pseudomonas spp.) that are viable and maize as a model plant. These authors found that inoculated
with a greater chance of environmental colonization, resulting plants had an assemblage pattern similar to those found in
in reliable functional outcomes. One approach is to target sugarcane, which demonstrates a successful colonization of
keystone taxa (i.e., microbial taxa that are highly connected the synthetic community. However, Armanhi et al. (2018)
or highly influential on the community) in a pre-existent or conducted their SynCom assembly by choosing highly abundant
artificially built microbiome (Banerjee et al., 2018). These taxa bacterial groups, and we propose a selection based on
provide an appealing target for microbial screening, followed microbe-microbe interactions, functional traits (e.g., nutrient
by isolation and whole genome sequencing to identify their solubilization/mineralization) and (or) colonization abilities
functional capabilities (Kong et al., 2018). Consequently, their (e.g., production of antimicrobial compounds). Moreover,
role in regulating the growth and function of other members biofertilizers can be developed with SynComs designed with
of the microbiome can be exploited to enhance specific high functional redundancy, in order to increase environmental
desired functions. adaptability and overcome some of the challenges of products
An important tool for identifying key taxa and developing currently available in the market.
ecosystem-wide dynamic models is through network analyses.
Based on high-throughput sequencing data, these networks
provide an overview of microbial assemblages and microbe- Personalized Microbial Inoculants and
microbe interactions. With network centrality metrics, they can Plant Prebiotics
allow to further detect microbial taxa that hold key topological Inspired by the concept of personalized diagnosis in medicine,
positions within the network (Toju et al., 2018b). Together, Schlaeppi and Bulgarelli (2015) proposed a similar strategy in
detecting ecologically significant microbial interactions, with agricultural systems. This strategy consists on customizing tools
proper experimentation, will provide powerful methods in such as microbial inoculants into farming practices. Similar to
developing new biofertilizers. fertilizer consultants that advise farmers on application strategies,
Bell et al. (2019) proposed a customizable field-scale microbial
Creating Synthetic Communities inoculant that, with appropriate implementation, could have
Recent culture independent techniques and new culture long-lasting effects. Considering that soil conditions might
collections have paved the way for developing artificially change dramatically over short distances (Peukert et al., 2016),
constructed communities, also known as “artificial microbial product development strategies of “one formulation applied
consortia” (AMC) or “synthetic communities” (SynComs). for all fields” seems unrealistic. One strategy is the on-farm
Here, core microbiomes are used to recreate the structure and production of mycorrhizae-based inoculants, in which studies
function of the microbiome. A great advantage of SynComs have shown their effects on potato (Douds et al., 2007; Goetten
studies is that it allows for a detailed evaluation under controlled et al., 2016) and eggplant (Douds et al., 2017) growth and
conditions, in which members can be added, eliminated, or nutrition. These locally produced inoculants often have low costs
substituted as needed (Vorholt et al., 2017). These studies can and are applied shortly after production, without the need of
also help to elucidate different aspects of the spatial structure, shipping and storage (Douds et al., 2005). Yet, it is important
microbial social interactions and how phenotypes interact and to consider how these products will be feasible or cost-effective
compete for space (Rodríguez Amor and Dal Bello, 2019). Yet, by on a global scale. A good starting point could be establishing an
definition, SynComs attempt to emulate the natural microbiome optimal range for biofertilizer performance, in which inoculants
with less complexity, retaining only the indispensable microbial would be introduced to conditions best resembling the soils
taxa, which could pose its own limitations (Vorholt et al., they were isolated from. Here, different formulations can be
2017; Satyanarayana et al., 2019). For example, SynComs with designed for particular soils and(or) plant-root systems with
lower complexity might bypass important associations or the incorporation of certain aspects of precision farming, thus
inter-relationships, which might be critical at the functional identifying areas in a particular field that might be more suitable
level and, therefore, unsuitable for field applications. Highly to one formulation or another.
complex SynComs, on the other hand, have their own designing Another strategy is to use root exudates to stimulate the
limitations but a better chance of keeping associations intact beneficial plant-associated microbiota. These exudates consist
(Satyanarayana et al., 2019). Despite its limitations, these predominately of sugars and organic acids, but also flavonoids,
reduced-complexity systems are particularly useful when a amino acids, fatty acids, hormones, antimicrobial compounds,
metabolic pathway is either too energy intensive or too complex and vitamins (Bulgarelli et al., 2013). They can serve as growth
to be accomplished by a single or few taxa. substrates or signals for suitable microbes that strongly influences
In plant sciences, SynComs were first introduced in studies rhizosphere microbiome composition and dynamics (Philippot
using Arabidopsis thaliana under gnotobiotic conditions (Bai et al., 2013; Mitter et al., 2017; Sasse et al., 2018).
For example, benzoxazinoids (BXs) are major secondary rhizosphere is an important trait that prevents microorganisms
defense metabolites in the Poaceae family (e.g., maize, wheat, from being detached from plant roots by various natural
and barley) that are typically produced during relatively early processes (Velmourougane et al., 2017).
plant growth stages (Cotton et al., 2019). Benzoxazinoids and In recent years, biofilmed biofertilizers (BFBFs) (i.e.,
their breakdown products are known to be biocidal to some biofertilizers containing microbial communities capable of
soil-borne bacteria and fungi and act as important regulators of forming biofilms) have emerged as a new inoculant strategy to
belowground plant–microbe interactions (Schütz et al., 2019). improve biofertilizer efficiency and sustain soil fertility (Parween
Despite their allelochemical properties, studies by Neal et al. et al., 2017). The idea behind BFBFs is that biofilm formation will
(2012) revealed that BXs may act as recruitment signals for create a more suitable environment for biofertilizers to compete
Pseudomonas putida KT2440 in maize plants. In addition, P. with resident organisms and to cope with the heterogeneity of
putida has been previously studied for their ability to solubilize biotic and abiotic factors in soil (Ünal Turhan et al., 2019). For
phosphate and thus promote growth of leguminous (Rosas et al., example, several studies have shown that biofilmed biofertilizers
2006) and maize (Sarikhani et al., 2020) plants. Hence, BXs could augmented P-solubilization (Swarnalakshmi et al., 2013), N2
be exploited to recruit beneficial microbes such as P-solubilizing fixation (Wang et al., 2017), siderophore production (Ricci
P. putida in field conditions. et al., 2019), and Zn solubilization (Triveni and Jhansi, 2017). In
Coumarins are a family of plant-derived secondary addition, studies by Kopycińska et al. (2018) highlighted the role
metabolites exuded by plants that have been extensively of biofilm formation, by exopolysaccharides (EPS) production,
studied for their role in induced systemic resistance (ISR) in Rhizobium leguminosarum during Zn stress. These authors
(Stringlis et al., 2018; Pascale et al., 2020). However, Tsai and found that EPS-deficient R. leguminosarum mutants were
Schmidt (2017) reported their involvement as Fe-mobilizing more sensitive to Zn exposure, whereas cell viability and root
compounds in response to Fe deficiency of dicotyledonous attachment were significantly higher in EPS producing strains.
plants. Moreover, Voges et al. (2019) demonstrated the role of Multi-species biofilms were also found to be more resilient
Fe-mobilizing coumarins in structuring the A. thaliana root in comparison to single-species biofilms (Velmourougane et al.,
bacterial community by inhibiting the growth of Pseudomonas 2017). In fact, natural rhizobacterial biofilms are often in mixed
spp. via a redox-mediated mechanism. Other molecules, such as communities with interspecies interactions. This assembly is
triterpenes, can also promote the enrichment of Bacteroidetes usually more advantageous than single planktonic cells, with
and the depletion of Deltaproteobacteria in A. thaliana (Huang optimal and maximal use of nutrients and resources (Nayak
et al., 2019). Similarly, Koprivova et al. (2019) reported et al., 2020). For example, fungal–bacterial biofilms have been
that a specific concentrations of plant derived camalexin shown to enhance nutrient uptake and environmental stress
concentration is necessary for proper interaction with a plant tolerance compared to mono- or mixed-cultures of no biofilm-
growth-promoting Pseudomonas sp. strain. forming microorganisms (Hassani et al., 2018). Taktek et al.
Multiple lines of evidence show that root exudates could (2017) studied two hyphobacteria (Rhizobium miluonense and
be used as compounds to stimulate the growth of beneficial Burkholderia anthina) and two mycorrhizobacteria (Rahnella
microbiota, rather than introducing microbes by inoculation. A sp. and Burkholderia phenazinium) that strongly attaches to
similar approach was proposed by Arif et al. (2020), in which the surface of the arbuscular mycorrhizal fungus Rhizoglomus
the authors suggested that particular soil amendments could irregulare. These authors demonstrated that B. anthina can
act as “prebiotics” to promote microbial functions. Qiu et al. strongly adhere to abiotic and biotic surfaces and allow a higher
(2019) also suggested that synthesized compounds can be added phosphate solubilization than other isolates tested. Beneficial
to crops to attract or favor particular microbes. Yet, we propose inter-kingdom biofilm formation were also reported in Bacillus
that these “plant prebiotics” could be used in combination with sp. with Gigaspora margarita (Cruz and Ishii, 2012) and
microbial inoculants to enhance biofertilizer efficiency. By acting Pseudomonas fluorescens with Laccaria bicolor (Noirot-Gros
as signaling molecules, these compounds could potentially attract et al., 2018).
introduced microbes to the rhizosphere, thus giving them an Biofilmed biofertilizers have potential applications to
advantage over other microorganisms for early colonization. improve ecosystem functioning and sustainability, which
includes enhancing soil fertility and protecting the host plant
Biofilmed Biofertilizers under adverse conditions. However, biofilms are known to be
Biofilms consist of associated microorganisms, either from a problematic in many industrial settings as they often clog pipes
single or multiple species, adhering to the biotic or abiotic and tubing (Vlamakis et al., 2013). Consequently, additional
surfaces in a self-produced matrix of extracellular polymeric studies are needed to test BFBFs efficiency at a field scale and to
substances (EPS) (Rana et al., 2020). This matrix provides determine optimal processes for a large-scale production and
the structure and protection by which microbes have the reliable results.
ability to chemically link with each other by quorum sensing
(QS) and work as one unit (Li and Tian, 2012; Vlamakis New Formulations and Delivery Methods
et al., 2013). In soils, microbial communities such as bacteria Following the selection of microorganisms and their functions, a
and fungi can form biofilms on abiotic surfaces such as ore suitable formulation is required to ensure microbial cell viability
(minerals), water-air interfaces, and dead organisms (Rekadwad during storage and application. In fact, most governments
and Khobragade, 2017). Moreover, biofilm formation in the regulate quality standards mandating a minimum number of
viable cells and a threshold for any potential contaminants non-entrapped cells. However, a few drawbacks still limit the
(e.g., chemical or microbial) (Herrmann et al., 2015; García de use of these formulations at a large-scale in agricultural systems.
Salamone et al., 2019). Hence, different bioformulations have For example, most natural polymers are heat sensitive and with
been developed and are broadly divided into those using solid lower mechanical strength compared to synthetic polymers (Zhu,
materials as carriers or liquid formulations. 2007). In addition, alginate can be relatively costly and the
The most commonly used solid carriers are peat, rock porosity of alginate particles could be a limiting factor for the
phosphate, charcoal, lignite, vermiculite, clay, diatomaceous biofertilizer industry (Reis et al., 2006; Sahu and Brahmaprakash,
earth, talc, cellulose, and polymers such as xanthan gum 2016).
(Mishra and Arora, 2016). Liquid formulations, also known A new approach for developing formulation methods is
as flowable or aqueous suspensions, consist of microbial by using fluid bed or fluidized bed dryer (FBD) to increase
suspensions in water, oils, or emulsions (Mondal and Dalai, inoculant survival rate and reduce contamination. Fluid bed
2017). In addition, bioformulations may contain additives such dryer has been extensively used by the pharmaceutical and
as methyl cellulose, starch and silica gel to improve their food industry to reduce the moisture of powders and granules
physical, chemical, and nutritional properties (Macik et al., 2020). (Dewettinck and Huyghebaert, 1999). In this process, particles
The main disadvantages of liquid bioformulations are that the to be coated are maintained suspended against gravity in an
metabolic activity of beneficial microbes decrease rapidly after upward flowing air stream causing them to behave as a fluid
manufacturing and they often have higher contamination risks (Sahu and Brahmaprakash, 2016). Then, the coating material is
(Kaminsky et al., 2019; Macik et al., 2020; Vassilev et al., 2020). On sprayed through a nozzle onto particles and electrical heaters are
the other hand, solid formulations (e.g., powders and granules) employed for drying the material (Schoebitz et al., 2013). One
are challenging for non-sporulating bacteria, as desiccation of the main advantages of this process is that it operates in a
disrupts cell membranes, causing cell death and overall loss of temperature of ∼37 to 40◦ C, which is milder than spray-drying
viability during rehydration (Berninger et al., 2018). This can lead and more suitable for mesophilic organisms (Sahu et al., 2018).
to major setbacks for product commercialization. Two strategies In fact, Gangaraddi and Brahmaprakash (2018b) reported longer
to overcome these limitations are using microbial encapsulation shelf-life of Rhizobium spp. inoculants in a FBD formulation,
with polymeric hydrogels and drying methods using a fluid bed in which cell viability was maintained for up to 120 days.
dryer (FBD). Higher cell viability using FBD have also been shown for
Polymeric hydrogels consist of crosslinked polymers chains biocontrol (Larena et al., 2003; Sabuquillo et al., 2006; Gotor-
with high affinity for water that are used for a variety of Vila et al., 2017) and for plant growth-promoting (Gangaraddi
technological applications (Kobayashi, 2018). These hydrogels and Brahmaprakash, 2018a) inoculants. In spite of these results,
provide: (i) an aqueous environment that helps maintain the the use of FBD technology in microbial inoculant formulations
biological function of the encapsulated material and (ii) a is not common. Future studies are still needed on optimizing
diffusion barrier that allows the passage of molecules with temperature cycles of FBD for inoculant formulations and to
a given size threshold (Pérez-Luna and González-Reynoso, assess survival rates after field applications. Yet, both methods
2018). Several naturally occurring (e.g., polysaccharides) and using alginate or FBD have promising effects in reducing
synthetic (e.g., polyacrylamide, polyurethane) polymers have formulation inconsistency by preserving microbial cell density
been widely used for microbial encapsulation; yet, alginate has during storage. Furthermore, these techniques may open new
been particularly attractive specially in biomedical applications possibilities to extend shelf-life of biofertilizers containing non-
due to its structural similarity to extracellular matrices of living spore forming Gram-negative bacteria.
tissues (Gasperini et al., 2014). Alginate is a polysaccharide
derived from different brown algae (e.g., Phaeophyceae) and BIOSAFETY OF BIOFERTILIZERS
bacteria (e.g., Azotobacter and Pseudomonas) (Lee and Mooney,
2012), and its main advantages are high biocompatibility in As discussed in previous sections, biofertilizers have great
supporting cell survival, low toxicity and ease of gelation potential to replace chemical inputs in agricultural systems
(Gasperini et al., 2014). but still face several challenges in terms of technical reliability
In biofertilizer applications, microbial cell entrapment with and accessibility to farmers. Yet, an important consideration is
alginate allows a gradual and controlled release of microbial their potential impact on both human and ecosystem health.
inoculants in the soil (Sahu and Brahmaprakash, 2016). The Due to the extensive nature of these risks, we believe that all
sticky nature of alginate may also help microbial cells to easily inoculant research and development should be assessed through
adhere to seeds and resist to environmental stresses (Nayak a “One Health” approach that regards plant, animal, human,
and Mishra, 2020). Lopes et al. (2020) used alginate beads for and ecosystem health (van Bruggen et al., 2019). Currently, our
encapsulating plant growth-promoting Trichoderma spp., and understanding of both the introduced microorganism/s and the
found higher survival rates in freeze-dried encapsulated cells complex interactions that occur in the plant-soil interface is still
at different storage temperatures. In addition, studies using limited to fully diagnose the risk posed by a specific product.
microbial cell entrapment with alginate have shown higher PGP However, research efforts have been made to fill knowledge gaps
rates on cotton (He et al., 2016), maize (Pitaktamrong et al., and to elaborate guidelines for assessing risks associated with
2018), and hybrid cabbage (Stella et al., 2019) compared to different inoculants (Vílchez et al., 2016). Understanding the
mechanisms behind successful PGP is as important as properly potentially pathogenic and mutualistic members of genus or
assessing the risks associated with the microorganisms that will species (Martínez-Hidalgo et al., 2018; Keswani et al., 2019).
be introduced in agricultural systems in a large scale. Another crucial step is understanding the role of horizontal gene
transfer in pathogenicity (Dobrindt et al., 2004), particularly
Human Health Risks among members of the same species or strain. This information
The plant-soil interface hosts a vast number of genetically and will allow to develop proper screening tests which could be
functionally diverse microorganisms, some of which interact with followed by toxicity and pathogenicity testing on model hosts
the plant in different ways (beneficial, neutral, and pathogenic). such as plants or nematodes (Martínez-Hidalgo et al., 2018).
Even though these interactions can lead to completely different However, in the case of host-specific pathogens, such as some
outcomes in terms of plant fitness, they are known to share many Burkholderia spp., model hosts might be insufficient to discard
features, to the extent that some symbiotic microbes could switch potential risks for humans (Eberl and Vandamme, 2016).
to a parasitic behavior with the same host (Kogel et al., 2006). For all the above mentioned, it is clear that proper biosafety
In the last decades, various root-associated bacteria, some of screening of any PGPB strain should become a standard practice
them studied for their PGP traits, were found to be opportunistic in biofertilizer production, ensuring the safety of the product
plant and human pathogens (Berg et al., 2013). Potential before exposing personnel, consumers, and natural resources
human pathogenic bacteria can be found among several genera, (Berg et al., 2013; Keswani et al., 2019). More research is
including Burkholderia, Pseudomonas, Rhodococcus, Serratia, needed on potential allergens (Keswani et al., 2019) and fungal
Acinetobacter, Stenotrophomonas, Enterobacter, Ochrobactrum, biofertilizers, including AMF, which might not be directly
Klebsiella, Ralstonia, and Bacillus (Martínez-Hidalgo et al., harmful for humans but could carry undesired microbial species
2018; Keswani et al., 2019). A well-studied case is that of in their formulation (Agnolucci et al., 2019). Moreover, it is
the Burkholderia cepacia complex, a group of phenotypically also important to understand the environmental conditions that
associated bacterial species which have known PGP traits, could promote the proliferation of opportunistic pathogens.
including N2 -fixation, but can also be opportunistic human For example, while some characteristics of the rhizosphere
pathogens (Chiarini et al., 2006; Eberl and Vandamme, 2016). environment could be favoring opportunistic pathogenic bacteria
Another intensively debated bacterial genus is Pseudomonas, (e.g., high nutrient availability, UV protection), others, such as
which encompasses several PGP species (e.g., P. fluorescens, high microbial diversity, could limit their survival (Matos et al.,
P. putida, P. putrefaciens, P. stutzeri, and P. pseudoalcaligenes) 2005; Mendes et al., 2013). Finally, there is a need for improved
but also the pathogenic species P. aeruginosa, an opportunistic consistency when evaluating risk and establishing regulatory
pathogen causing respiratory tract infections in humans (Mendes frameworks such as the Risk Groups (Europe) and Biosafety
et al., 2013). Level or BSL (United States) (Vílchez et al., 2016). Vílchez et al.
Currently, the majority of commercial biofertilizers consist (2016) developed an evaluation system, the “Environmental and
of formulations of N2 -fixing organisms (e.g., Actinorhizobium Human Safety Index (EHSI)” based on a panel of tests which
spp., Azospirillum spp., Azotobacter spp., and Rhizobium spp.), could be used to evaluate the safety of PGP bacteria in an
which have a low health risk and a history of safe application objective and reliable manner, encompassing not only human
(Martínez-Hidalgo et al., 2018; Sessitsch et al., 2019). Yet, other but also environmental health. More effort must be invested in
bacterial species or strains which could provide useful functions similar projects, with a special emphasis on international and
for agriculture could also pose a biosafety threat. For instance, interdisciplinary exchange and cooperation.
Actinobacteria are thought to have low pathogenic risk, but some
species such as Streptomyces somaliensis can cause disease in
humans (Martínez-Hidalgo et al., 2018; Olanrewaju and Babalola, Environmental Health Risks: Effects on the
2019). In other cases, the presence of pathogenic species or Resident Biota
strains within a taxonomic group can lead to drastic measures Ideally, a biofertilizer should cause a minimum and/or controlled
that would not be necessary with the proper testing methods impact in terms of dispersion, persistence, alteration of
and risk evaluation protocols. The B. cepacia complex was microbial function and biogeochemical cycling, and alteration
restricted for field application in the United States (Martínez- of macroflora and macrofauna (Bashan et al., 2014). A major
Hidalgo et al., 2018), even though its pathogenicity and ecology concern is the effect of the introduced microorganism/s
were found to be variable among species (Chiarini et al., 2006). on the resident microbiome, which can occur from direct
The evaluation of pathogenicity and risk associated with a ecological interactions, either synergistic or antagonistic (e.g.,
particular species or strain is unclear. More research is needed competition, inhibition), as well as horizontal gene transfer
to identify genotypic and phenotypic differences between a plant (Glick, 2020; Mawarda et al., 2020). Introduced microorganisms
or soil opportunistic pathogens and their clinical counterparts can also modify resident microbial communities indirectly, by
(Mendes et al., 2013; Martínez-Hidalgo et al., 2018). Genetic modulating plant physiology and morphology. For example,
analyses could provide information about presence or absence some PGP are known to modify root architecture and exudation
of known virulence factors such as quorum sensing, motility, (Vacheron et al., 2013), which can alter rhizosphere communities
siderophore production, and lipopolysaccharide biosynthesis (Jones, 1998; Saleem et al., 2018). In mixed plant communities,
(Guttmann and Ellar, 2000; Eberl and Vandamme, 2016). In this indirect effects on the resident microbiome could also be
sense, a powerful tool is whole genome sequencing to compare expected if the introduced microorganism induces changes in
plant diversity and composition, as was observed with some AMF The impact that introduced microbes may have on the
inoculants (Hart et al., 2018; Keswani et al., 2019). resident microbial communities will depend to some extent
Inoculation of rhizobia, widely utilized in biofertilizers, on their abundance, survival, and permanence in the system
have shown significant impacts on soil and plant-associated (Ambrosini et al., 2016). This means that the same characteristics
microbial communities, as found in soybean (Zhong et al., that will help guarantee a successful plant growth promotion,
2019) and alfalfa (Schwieger and Tebbe, 2000) crops. These are also the ones increasing the risk for invasion. Yet, not
effects were not limited to the rhizosphere; field inoculation enough studies focus on the effect of mass and repetitive
of Phaseolus vulgaris with two indigenous rhizobia strains inoculation, or effects in the long term or in subsequent crops
(separately or combined) modified the structure and increased (Trabelsi and Mhamdi, 2013; Mawarda et al., 2020). According
the phylotype richness of bacterial communities in the bulk to Hart et al. (2018), long-term effects are also important for
soil (Trabelsi et al., 2011). Changes in microbial structure can AMF inoculants, although their complex genetic organization
result from both positive and negative interactions of rhizobia will definitely challenge the assessment of their establishment
with the rhizosphere microbiome. Azospirillum, a bacterial genus and persistence. These effects are particularly concerning if
characterized by free-living organisms with N2 -fixing capabilities we consider that inoculation effects could remain even after
among other PGP traits, has shown variable effects on the the introduced microbial population decreases (Mawarda et al.,
resident microbiome (Trabelsi and Mhamdi, 2013). Inoculation 2020). One of the mechanisms behind these “legacy” effects is
of maize with A. lipoferum induced a shift in the composition through plant-soil feedbacks, something more likely to occur
of rhizosphere bacterial communities which lasted for at least when the introduced microorganism is symbiotic or has a high
one month (Baudoin et al., 2009). Yet, variable results were affinity for a specific plant (e.g., a non-target plant present in the
observed when inoculating the same or other crops with agroecosystem) (Ambrosini et al., 2016; Keswani et al., 2019).
A. brasilense (Herschkovitz et al., 2005; Lerner et al., 2006; The variable effects observed on the resident microbiome
Correa et al., 2007), even though this bacterium can induce when introducing a microorganisms via inoculation suggest the
physiological and morphological changes in the root system. outcome is driven by several factors, including the host plant
According to Trabelsi and Mhamdi (2013), effects of Azospirillum (Marschner and Timonen, 2005). For example, Correa et al.
inoculation on rhizosphere microorganisms is likely driven by (2007) found that the plant genotype modulated the genetic and
N dynamics, although evidence suggests that a wide array of physiological response of phyllosphere and rhizoplane bacterial
factors are involved. While rhizobia and Azospirillum have been communities to A. brasilense seed inoculation. In another
more widely studied regarding their effects on the resident study, the response of rhizosphere bacterial communities to
microbiome, research on other taxa such as Pseudomonas sp. A. brasilense changed with the crop growth stage, being more
remains limited, even though they could potentially modify both affected at jointing than grain-filling stage (Di Salvo et al.,
bacterial and fungal communities (Andreote et al., 2009; Gao 2018). On the other hand, the resident microbiome might
et al., 2012). present different susceptibility and buffering capacity levels
Among fungal biofertilizers, those based on AMF are the most depending on its diversity (Eisenhauer et al., 2013; Trabelsi
widespread and commercially available, even though ecological and Mhamdi, 2013) and the presence of specific antagonists
risks of field application are not being properly assessed (Hart or synergistic taxa (Mar Vázquez et al., 2000; Asiloglu et al.,
et al., 2018). Inoculation with foreign AMF can affect native AMF 2020). Similarly, environmental conditions may play a key
communities, for example displacing them and reducing their role regulating the impact of introduced microorganisms, as
diversity (Koch et al., 2011) or modifying their composition (Jin observed for soil moisture (He et al., 2019b; Monokrousos
et al., 2013a), although a response in the native AMF community et al., 2020) and light intensity (Marschner and Timonen,
is not always observed (Antunes et al., 2009). In the study by Jin 2005).
et al. (2013b), a diverse AMF inoculum had less beneficial effects Overall, most studies analyzing the impact of biofertilizers
on plant fitness but had a lower impact on the composition of seem to focus on structural aspects and not enough on
subsequent AMF communities. Besides native mycorrhizal fungi, functionality (Trabelsi and Mhamdi, 2013). Understanding the
introduced AMF can disturb other microbial communities in functional implications of those changes is crucial, since they
soil, particularly those surrounding their extraradical mycelium, will directly impact ecosystem functioning and health. Multi-
(i.e., the mycorrhizosphere) (Trabelsi and Mhamdi, 2013). So omics and data analysis are key tools to begin to understand
far, the effect of AMF on soil microbial communities seems to the complex dynamics taking place and to predict microbial
be variable and modulated by several factors (Marschner and response under natural conditions (Ambrosini et al., 2016;
Timonen, 2005; Cavagnaro et al., 2006; Monokrousos et al., Timmusk et al., 2017). Another question that remains is
2020). Remarkably, bacteria inhabiting the mycorrhizosphere, how persistent the environmental impact of the introduced
some of which may already be present in commercial inoculants, microbes is (i.e., long-term and legacy effects). Moreover,
have shown PGP activity and are thought to act synergistically further research is needed in the specific case of genetically
with AMF (Agnolucci et al., 2019). Lastly, non-AMF fungal modified microorganisms, including effects of metabolic load
inoculants have been less studied but there is some evidence (Glick, 2020), and risks of horizontal gene transfer and
for endophytic fungi (Casas et al., 2011; Rojas et al., 2016) and dispersion (Hirsch, 2004; Bellanger et al., 2014). Diverse
Trichoderma spp. (Jangir et al., 2019) to induce changes in local inoculants could be a safer alternative in terms of environmental
microbial communities. impact, as suggested by studies on AMF or Bacillus spp.
inoculation (Jin et al., 2013a; Gadhave et al., 2018). Still, CONCLUSIONS AND FUTURE
further research is needed to fully understand the impact PERSPECTIVES
of different types of mixed inoculants (either based on
same species, different species or different strains) on the The global biofertilizer market has an estimated value of 2.3
resident microbiome. billion US dollars and it is projected to increase to 3.9 billion in
FIGURE 2 | Overview of biofertilizer development workflow from potential candidate microorganisms to commercial applications with four novel approaches:
single-strain inoculant obtained using emerging culture-based methods (e.g., culturomics), synthetic microbial communities (SynComs) obtained from a bottom-up
approach, whole microbiomes recovered from natural or engineered ecosystems (top-down approach), and prebiotics obtained from root exudates. Following the
initial stages of bioprospecting and in vitro testing, selected inocula and/or prebiotics require a proper formulation to ensure shelf life and protection. Finally, product
pre-commercialization steps include in planta trials under controlled (growth chamber/greenhouse) and uncontrolled (field) conditions, production scale-up to a
commercial scale, proper biosafety screening tests (e.g., toxicity and pathogenicity), and compliance with existing regulations. Created with BioRender (https://
biorender.com/).
2025 (Marketandmarkets, 2020). Despite their great potential and to ensure their safety before exposing personnel, consumers and
long-term effects, biofertilizer products still face major challenges natural resources. Moreover, continued studies on ecological
limiting their use in agricultural settings. These are often interactions and how plants shape their microbiome in
associated with limited shelf-life and the survival of inoculated agricultural systems are still essential. This is particularly critical
strains in vastly different environments. in the context of climate change, where key biogeochemical
In this review, we highlighted the application of multi-omics processes carried out by soil microorganisms may be affected.
approaches and emerging technologies in biofertilizer Due to the complexity and genetic diversity within the soil
development (Figure 2). As discussed by Saad et al. (2020) and plant microbiome, it is unlikely that one formulation will
and Toju et al. (2018a), keystone taxa provide an appealing be effective for all fields. Yet, it is unfeasible and unrealistic to
target to optimize the outcomes of biofertilization due their design specific biofertilizers for each particular field. For this
role in regulating the growth/function of other members in reason, in agreement with Bell et al. (2019), we suggest that
the plant microbiome. We propose that these taxa and other continuous product design, refinement, and validation should
members of the core microbiome could be further explored be oriented toward optimal and sub-optimal environmental
to manipulate microbiomes or design synthetic microbial ranges for microbial products (i.e., crop, climate, soil type,
communities (e.g., SynComs). At the same time, emerging and agricultural practices). Finally, significant resource inputs
culture-based methods (e.g., “culturomics”) can be used to from both public and private sectors are needed to fill critical
discover novel isolates with biofertilizer applications. As an knowledge gaps in the field. This effort must be accompanied
alternative, or in combination with, we suggest the use of “plant by the encouragement of regulatory agencies and policy makers
prebiotics,” that act as signaling molecules to attract beneficial supporting sustainable practices and biofertilizers.
microbes, thus enhancing biofertilizer efficiency. These studies
can be further integrated into a global database systematizing AUTHOR CONTRIBUTIONS
different outcomes, environmental conditions, targeted plant
genotypes, soil types, and growing seasons. EKM, MT, and DO collected literature and wrote the
The success of biofertilizers, however, not only depends on manuscript. EKM edited the manuscript and MT designed
selecting specific microorganisms or functions, but also on the figures. JJG and KED provided critical feedback. All authors
developing new formulations to ensure the survival of inoculated conceived and planned the scope, and approved the final
strain(s). Here, we reviewed different methods in which version manuscript.
bioformulations could be improved by using biofilm-producing
strains, microencapsulation with alginate, and processes based FUNDING
on fluidized bed dryer (FBD). Ideally, new technologies should
target carriers and additives that are cost-effective and easy to use This work was supported by Food from Thought, a program
but, most importantly, able to support a higher number of viable funded by Canada First Research Excellence Fund (CFREF)
cells during storage and application. and the Natural Sciences and Engineering Research Council
Simultaneously, the biosafety of inoculated microbes should (NSERC). Funding was provided by a MITACS Elevate
be assessed through a “One Health” approach. This step includes Post-doctoral Fellowship (EKM) and the Canada Research Chairs
proper screening tests (e.g., toxicity and pathogenicity testing) Program (KED).
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synthetic root microbiome. Proc. Natl. Acad. Sci. U.S.A. 116, 12558–12565. access article distributed under the terms of the Creative Commons Attribution
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microbiome research. Cell Host Microbe 22, 142–155. doi: 10.1016/j.chom.2017. practice. No use, distribution or reproduction is permitted which does not comply
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published: 19 February 2021

Rethinking Crop Nutrition in Times of

Global population growth poses a threat to food security in an era of increased

Received: 15 September 2020

Challenges Potential solution(s)

Practical Aspects New Culture-Dependent Methods

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