The Current Status On The Taxonomy of Pseudomonas Revisited, Peix2018

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The current status on the taxonomy of Pseudomonas revisited: An

update
Alvaro Peix, Martha-Helena Ramírez-Bahena, Encarna Velázquez
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DOI: doi:10.1016/j.meegid.2017.10.026
Reference: MEEGID 3314
To appear in: Infection, Genetics and Evolution
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Revised date: 28 October 2017
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The current status on the taxonomy of Pseudomonas revisited: an update
Alvaro Peix1,2, Martha-Helena Ramírez-Bahena3 and Encarna Velázquez2,3
1. Instituto de Recursos Naturales y Agrobiología. IRNASA-CSIC. Salamanca.

Spain.
2. Unidad Asociada Universidad de Salamanca- CSIC „Interacción Planta-
Microorganismo‟. Salamanca. Spain
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3. Departamento de Microbiología y Genética and Instituto Hispanoluso de
Investigaciones Agrarias. Universidad de Salamanca. Spain.
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*Corresponding author: Encarna Velázquez. Departamento de Microbiología y
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Genética. Lab. 209. Edificio Departamental de Biología. Campus Miguel de
Unamuno. 37007 Salamanca. Spain. Phone: +34 923 294532. Fax number: +34 923
224876. E-mail: evp@usal.es
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Running title: Pseudomonas taxonomy

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Abstract
The genus Pseudomonas described in 1894 is one of the most diverse and ubiquitous
bacterial genera which encompass species isolated worldwide. In the last years more
than 70 new species have been described, which were isolated from different
environments, including soil, water, sediments, air, animals, plants, fungi, algae,
compost, human and animal related sources. Some of these species have been isolated
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in extreme environments, such as Antarctica or Atacama desert, and from
contaminated water or soil. Also, some species recently described are plant or animal
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pathogens. In this review, we revised the current status of the taxonomy of genus
Pseudomonas and the methodologies currently used for the description of novel
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species which includes, in addition to the classic ones, new methodologies such as
MALDI-TOF MS, MLSA and genome analyses. The novel Pseudomonas species
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described in the last years are listed, together with the available genome sequences of
the type strains of Pseudomonas species present in different databases.
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Keywords: Pseudomonas; taxonomy; MLSA; genomes; MALDI-TOF MS

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1. The genus Pseudomonas: a brief historical review

The genus Pseudomonas was described at the end of 19th century (Migula, 1894)
when descriptions of genera were based on the macro and microscopic morphologies,
a practice universally accepted by the microbial taxonomists (Cohn, 1872). Already in
the 20th century, the physiological characteristics were proposed as basic criteria for
bacterial taxonomy (Orla-Jensen, 1909). In the Bergey‟s Manual published in 1923,
several phenotypic characteristics were added to the morphology, Gram-stain,
flagellation type and metabolism with respect to the oxigen, in an attempt to
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differentiate the species of the genus Pseudomonas (Bergey et al., 1923).
When the techniques based on DNA began to make possible the use of genetic
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approaches in bacterial taxonomy (Marmur, 1961; Marmur and Dotty, 1961;
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Schildkraut et al., 1961), the DNA base composition (G+C) and the DNA-DNA
hybridization were the first techniques applied to Pseudomonas taxonomy (Colwell
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and Mandel, 1964; Colwell et al., 1965; Johnson and Ordal, 1968). This way, the G+C
content of all Pseudomonas species was included in the Bergey‟s Manual from 1974
(Doudoroff and Palleroni, 1974). Later, the pseudomonads were divided into five
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rRNA subgroups based on the measurements of RNA-DNA and this classification

was reported in the Bergey's Manual of Systematic Bacteriology published in 1984
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(Palleroni, 1984).
The deepest changes in bacterial taxonomy occurred in the 1980‟s, when Woese and
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collaborators proposed the analysis of the 16S ribosomal RNA gene sequences for the
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classification of bacteria placing the genus Pseudomonas into the Gamma

Proteobacteria (Woese et al., 1984). Nevertheless, the most relevant of these changes
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affecting the genus Pseudomonas began from the 2000‟s year onwards with a first
work compiling the sequences of the 16S rRNA gene of 128 Pseudomonas species
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carried out by Anzai et al. (2000), who showed that many species did not fit within
the Pseudomonas sensu stricto cluster, which contained the members of the rRNA
group I from Palleroni (1984). The members of the remaining rRNA groups were
splitted in more than 25 genera belonging to the classes Alpha, Beta and
Gammaproteobacteria (Peix et al., 2009; García-Valdés and Lalucat, 2016). These
changes were recorded in the edition of Bergey‟s Manual of Systematic Bacteriology
from year 2005, which changed from printed to on-line format in 2015 where each
genus constitutes an independent chapter. This new format will permit the information
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to be updated more frequently, which is currently essential taking into account that the
bacterial genera and species number is continuously increasing.
2. The recently described species: from 2009 onwards

In our previous review on Pseudomonas taxonomy we reported the species described
up to year 2009 (Peix et al., 2009). From this year onwards their number continues
increasing with the description of more than 70 new species (Table 1). Some of them
have been isolated from human related sources, such as 'P. saudiphocaensis' and 'P.
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saudimassiliensis', which were isolated from currency notes (Azhar et al., 2016) and
'P. massiliensis', isolated from a woman stool specimen (Bardet et al., 2017), or from
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animal sources, such as P. weihenstephanensis, P. helleri, P. lactis and P. paralactis
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isolated from cow's milk (von Neubeck et al., 2016, 2017), and P. coleopterorum
isolated from the bark beetle Hylesinus fraxini (Menéndez et al., 2015). Some recently
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described species were pathogenic for animals, such as the entomopathogenic P.
entomophila (Mulet et al., 2012) and the fish Dicologlossa cuneata pathogen P.
baetica (López et al., 2012), or for plants, such as P. cerasi, pathogenic for cherry
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trees (Kałużna et al., 2016), P. asturiensis, pathogenic for soybean (González et al.,
2013) and P. caspiana, pathogenic for citrics (Busquets et al., 2017). The remaining
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species were isolated from different sources, being the soil the major isolation source
with 30 novel Pseudomonas species isolated from this environment (Table 1). Some
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of the new Pseudomonas species recently described were isolated from plant related
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sources and have several in vitro plant growth promotion mechanisms. This way, P.
sagittaria and P. donghuensis, were found to produce siderophores (Liu et al., 2013;
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Gao et al., 2015), P. guariconensis and P. helmanticensis, could solubilize phosphate

(Toro et al., 2013; Ramírez-Bahena et al., 2014), P. endophytica was found to have
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several PGPR mechanisms and P. protegens and P. canadensis, were reported as

biocontrol agents (Ramette et al., 2011; Tambong et al., 2016). Other species were
isolated from extreme environments, as the case of P. guguanensis and P.
yangmingensis isolated from hot springs (Liu et al., 2013; Wong and Lee, 2014), P.
arsenicoxydans isolated in the Atacama desert (Campos et al., 2010) and the
psychrotrophic species isolated in Antarctic locations, P. extremaustralis (López et
al., 2009); P. deceptionensis (Carrión et al., 2011), P. prosekii (Kosina et al., 2013), P.
yamanorum (Arnau et al., 2015), P. gregormendelii (Kosina et al., 2016) and P.
versuta (See-Too et al., 2017). It is to be highlighted that all these novel species are
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phylogenetically very diverse. Such diversity is not surprising taking into account the
very heterogeneous habitats where these species were found, which reflects that
Pseudomonas is an ubiquitous genus. Considering that most environments remain still
unstudied from a microbiological point of view, it is to be expected that the number of
new Pseudomonas species will significantly increase in future years.
3. Current methods used in Pseudomonas taxonomy

The criteria used in Pseudomonas taxonomy has been previously reviewed (Peix et
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al., 2009; García-Valdés and Lalucat, 2016) and an exhaustive list of methods used in
Pseudomonas taxonomy is also included in the current edition of Bergey‟s Manual of
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Systematic Bacteriology (Palleroni, 2015).
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The phenotypic-based methods are still used not only for the characterization of new
Pseudomonas species, but also for their identification. The commercial systems used
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for identification of Pseudomonas species include kits of automatic read which are
still routinely used in many laboratories. Some of these kits, such as API 20NE, were
specifically designed for the identification of clinical Pseudomonas (Barr et al., 1989),
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but they fail in the identification of non-clinic species being only useful for
phenotypic characterization (Behrendt et al., 1999; Peix et al., 2003). By contrast, the
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Biolog Microbial Identification Systems, firstly the GN2 (GEN II) and currently the
GEN III plates, have been applied to the identification of Pseudomonas species
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isolated from non-clinical sources (Avidano et al., 2010; Janisiewicz and Buyer, 2010;
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Martin et al., 2011; Li et al., 2013; Liu et al., 2013; Akter et al., 2014). All these
systems are commonly used for the phenotypic characterization of novel
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Pseudomonas species (Palleroni, 2015).

Several chemotaxonomic characteristics are also useful for bacterial characterization
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being the quinone systems and the fatty acid profiles always included in Pseudomonas
species descriptions. The analysis of fatty acid profiles (FAMES) has also been
proposed as an identification method through the MIDI system (Mansfeld-Giese et al.,
2002; Chao et al., 2010; Janisiewicz and Buyer, 2010), particularly for the
identification of plant pathogenic strains (Lamichhane et al., 2010; Gitaitis et al.,
2012; Conner et al., 2013; Gumtow et al., 2013; Bozkurt et al., 2016; Webb et al.,
2016).
The SDS-PAGE, polyamine and siderophore profiles are not currently included within
the taxonomic markers needed for new species descriptions, but they are useful to
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differentiate among Pseudomonas species and therefore they have been included in
the description of some of them (Auling et al., 1991; Vancanneyt et al., 1996; Meyer
et al., 2002). For example, the SDS-PAGE has been used in the description of some
novel species, such as P. cuatrocienegasensis (Escalante et al., 2009) and P. prosekii
(Kosina et al., 2013). The polyamine patterns were used to differentiate the species P.
psychrotolerans (Hauser et al., 2004), P. knackmussii (Stolz et al., 2007) and P.
hussainii (Hameed et al., 2014). The siderotyping has been used to characterize novel
species, such as P. costantinii, which causes brown blotch disease in mushrooms
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(Munsch et al., 2002), P. salomonii, which causes 'Café au lait' disease in garlic
(Gardan et al., 2002), or the non-pathogenic ones P. palleroniana (Gardan et al.,
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2002) and P. protegens (Ramette et al., 2011).
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Despite the usefulness of the phenotypic and chemotaxonomic features in
Pseudomonas classification and identification, the most precise techniques for these
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purposes are the genomic-based procedures, which comprise nucleic acid
fingerprinting, particularly used for biodiversity analysis, and gene sequence analysis,
which can be used for biodiversity analysis and for phylogenetic and taxonomic
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studies. Although fingerprinting techniques such as amplified ribosomal DNA

restriction analysis (ARDRA), repetitive extragenic palindromic (REP),
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enterobacterial repetitive intergenic consensus (ERIC), bacterial repetitive BOX

elements (BOX) and randomly amplified polymorphic DNA (RAPD) were developed
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many years ago, they are still the most reliable techniques for biodiversity studies and
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currently they are profusely used to analyse Pseudomonas strains isolated from both
environmental and clinical samples (Auda et al., 2016; Bazhanov et al., 2016;
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Kalferstova et al., 2016; Keshtkar et al., 2016; Morales et al., 2016; Moretti et al.,
2016; Santoro et al., 2016; Streeter et al., 2016; Wu et al., 2016; Cohen et al., 2017;
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Kallufa et al., 2017; Rijaveca and Lapanje, 2017).

Regarding gene analysis, the 16S rRNA gene continues to be the basis of bacterial
classification allowing the differentiation of genus Pseudomonas from the remaning
genera of bacteria (Palleroni et al., 2015). Therefore, 16S rRNA sequence analysis is
mandatory in every description of novel bacterial species (Tindall et al., 2010).
Nevertheless, this gene is not discriminative at species level in several phylogenetic
groups of Pseudomonas and therefore, in the last decade, other protein codifying
genes have been added to the taxonomic and phylogenetic studies of this genus. These
genes are commonly analysed for the description of the new Pseudomonas species
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and a MLSA (multilocus sequence analysis) database (PseudoMLSA) has been

developed to compile multiple gene sequences of the type strains of species described
since 2008 (Bennasar et al., 2010). Considering the usefulness of MLSA to
differentiate among Pseudomonas species, in several recent works this approach has
been used for identification and phylogenetic and population analyses of plant
pathogenic (Chapman et al., 2012; Beiki et al., 2016; Newberry et al., 2016), clinical
(Cholley et al., 2014; Eusebio et al., 2015; Suzuki et al., 2016; Yonezuka et al., 2016;
Mulet et al., 2017) and environmental (Parejko et al., 2013) strains.
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Among the housekeeping genes proposed along the years for genus Pseudomonas
(reviewed by García-Valdés and Lalucat, 2016), the gyrB, rpoB, and rpoD genes are
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particularly useful in species delineation (Mulet et al., 2010; Gomila et al., 2015;
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García-Valdés and Lalucat, 2016), being the rpoD the most discriminative for this
purpose, followed by gyrB, which is also a powerful phylogenetic marker, and by the
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rpoB, the least discriminative marker among them (Mulet et al., 2010). Using
concatenated sequences of 16S rRNA, gyrB, rpoB and rpoD genes (MLSA), the most
comprehensive studies on the phylogenetic relationships of the different Pseudomonas
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species carried out to date, showed the existence of two main lineages, the P.
fluorescens lineage and the P. aeruginosa lineage (Mulet et al., 2010; Gomila et al.,
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2015; García-Valdés and Lalucat, 2016). According to these authors, the P.

fluorescens lineage comprises 6 phylogenetic groups: P. fluorescens, P. syringae, P.
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lutea, P. putida, P. anguilliseptica and P. straminea groups, where the biggest is the
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P. fluorescens group, which includes numerous subgroups. The P. aeruginosa lineage

includes 4 groups: P. aeruginosa, P. oleovorans, P. oryzihabitans and P. stutzeri
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groups (Mulet et al., 2010; Gomila et al., 2015; García-Valdés and Lalucat, 2016),
and, recently, a new group was defined, the P. pertucinogena group, which clusters
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separately from the two main phylogenetic lineages of Pseudomonas (P. fluorescens
and P. aeruginosa), (García-Valdés and Lalucat, 2016). In their analysis, these
authors also found that several Pseudomonas species clustered out of the 11 defined
groups, such as P. rhizosphaerae, P. caeni, P. luteola or P. duriflava. Now we have
performed a MLSA based on concatenated 16S rRNA, gyrB, rpoB and rpoD genes of
the species described from 2009 to date finding that they are distributed in almost all
the Pseudomonas groups previously defined by Mulet et al. (2010) and García-Valdés
and Lalucat (2016), with the exception of the P. lutea and P. oryzihabitans groups
(Fig. 2). However, some of these novel species could represent novel yet undefined
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groups, such as P. turukhanskensis, P. massiliensis, P. kuykendallii, P. salegens and

P. aestusnigri, as can be seen in Fig. 2. The phylogenetic analysis also shows that two
novel groups can now be defined, the P. rhizosphaerae group within the P.
fluorescens lineage, and the P. luteola group within the P. aeruginosa lineage.
Moreover, a novel lineage can be proposed, the P. pertucinogena lineage, which
includes the well consolidated “P. pertucinogena group” previously defined by
García-Valdés and Lalucat (2016) in which several of the new species group together.
The tree topology we inferred is in agreement with García-Valdés and Lalucat (2016),
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but using the same genes in MLSA analysis, Garrido-Sanz et al. (2016) excluded from
the P. fluorescens phylogroup the groups of P. anguilliseptica and P. straminea,
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placing them into P. aeruginosa phylogroup. These differences can be explained
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because they used a different concatenation placement of the genes and different
methods to infer the phylogeny, nevertheless they obtained a coherent topology for
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most groups showing similar phylogenetic relationships among them.
This fact also evidence the enormously complex phylogeny of genus Pseudomonas,
which contains more than 190 species to date
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(http://www.bacterio.net/pseudomonas.html). It is likely that in the future the current

genus Pseudomonas may be splitted in more than one genus, based on phylogenetic
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and chemotaxonomic analyses, if a thorough taxonomic revision of family

Pseudomonadaceae is performed.
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4. Modern approaches in Pseudomonas taxonomy: the omics era

In year 2003 Guttmacher and Collins published an opinion article in the New England
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Journal of Medicine entitled "welcome to genomic era" where they considered that
the genomic era began in 2003 with the complete sequencing of the human genome.
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However, the genome sequencing began many years before, concretely with the
sequencing of the first bacterial genome sequenced, the Haemophilus influenzae
genome in 1995 (Fleischmann et al., 1995). The post-genomic era also began in the
2000's decade when many genomes and metagenomes were sequenced leading to
great changes in Microbiology (Medini et al., 2008).
The comparison of whole genomes offers a more exact picture about the phylogenetic
relationships among bacteria facilitating the differentiation of bacterial taxa, although
the number of genomes is still low and it is not easy to conciliate the genomics with
the microbial taxonomy (Klenk and Göker, 2010). This objective was approached by
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the Genomic Encyclopaedia of Archaea and Bacteria (GEBA), which has been
developed in different phases and incorporates the sequences of many type strains of
bacteria and archaea (Wu et al., 2009; Kyrpides et al., 2014; Whitman et al., 2015).
The incorporation of the whole genomes to the systematics or taxonogenomics has
been proposed as a reliable tool for novel species description (Ramasamy et al.,
2014). This is currently applied mainly, but not only, to describe new species of
uncultured bacteria isolated from human related sources, constituting together
culturomics the new trend in clinical microbiology (Lagier et al., 2015).
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The first complete genome sequenced in the genus Pseudomonas was that of strain P.
aeruginosa PAO1 in 2000 (Stover et al., 2000) and in the same year an interactive
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database based on this genome was developed as a bioinformatic tool for
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Pseudomonas researchers (Croft et al., 2000). From this date, the number of whole
genomes of Pseudomonas species has been continuously increasing (Tables 2 and S1)
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and the databases of Pseudomonas genomes have been improved along the time
adding new tools to facilitate their use in gene searching, genome annotation and
genome comparison and analysis (Winsor et al., 2009, 2010 and 2016). The
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comparison and analysis of whole genomes is a good tool in Pseudomonas taxonomy

and ANI (Average Nucleotide Identity) or Genome-to-Genome Distance (GGDC)
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have been analysed in recently published descriptions of new species, such as P.

donghuensis, P. alkylphenolica, P. cerasi or P. versuta (Gao et al., 2015; Mulet et al.,
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2015; Kałużna et al., 2016; See-Too et al., 2017). It is currently widely accepted that
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the range threshold values of 94-96 % ANI similarity proposed by Richter and
Rosselló-Mora (2009) for delineation of bacterial species is equivalent to the 70%
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DNA-DNA hybridization classically established for experimental laboratory

procedures. In addition, the comparison of Pseudomonas whole genomes is a tool in
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epidemiological (Spencer et al., 2013; Snyder et al., 2013), plant interaction (Silby et
al., 2009; Loper et al., 2012; McCann et al., 2013; Nowell et al., 2016), diversity
(Silby et al., 2009; Jun et al., 2015) and environmental (Schwartz et al., 2015; Lidbury
et al., 2016) studies.
The rapid increase of the whole genome sequences available in databases in the last
decade has also favoured the development of genome mining methods focusing on the
search of bacterial metabolites (Ziemert et al., 2016). Currently, the genome analysis
is a good tool in the field of clinical microbiology (Thomsen et al., 2016; Houldcroft
et al., 2017), food microbiology (Deng et al., 2016; Ronholm et al., 2016; Walsh et
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al., 2017), phytopathology (Bull and Koike, 2015; Vinatzer et al., 2017) or agriculture
(Thao and Tran, 2016). The availability of many Pseudomonas whole genomes has
facilitated the genome mining (Winsor and Brinkman, 2014) to search antimicrobial
metabolites (Loper et al., 2008; van der Voort et al., 2015; Krzyżanowska et al.,
2016), enzymes (Ficarra et al., 2016; Sun et al., 2016) and diverse biological activities
(Garrido-Sanz et al., 2016). Nevertheless, this is a field still poorly studied in this
genus which should be further exploited.
Techniques based on protein analysis, proteomics, are also currently applied in
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bacterial taxonomy and within them, matrix-assisted laser desorption ionization time
of flight mass spectrometry (MALDI-TOF MS) is the most promising technique. It
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has been applied to bacterial identification, particularly for strains isolated from
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clinical sources (Angeletti, 2016). In the case of Pseudomonas, this methodology has
been applied to the identification of clinical isolates since the last decade when
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Degand et al. (2008) reported that Pseudomonas aeruginosa strains isolated from
cystic fibrosis patients were correctly identified by MALDI-TOF MS. From this date
onwards several works reported the identification of different Pseudomonas species
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isolated from these patients (Baillie et al., 2013) and from several clinical sources
(Seng et al., 2009; Jacquier et al., 2011; Fall et al., 2015; Lo et al., 2015; Mulet et al.,
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2017) and foods (Böhme et al., 2013; Vithanage et al., 2014; Höll et al., 2016). In
several works the accuracy of MALDI-TOF MS for identification of bacteria
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including Pseudomonas was compared with that of other methods concluding that it is
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comparable to the results of automatized phenotypic methods (Jamal et al., 2014).

MALDI-TOF MS allows the correct identification of Pseudomonas species,
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subspecies, genomovars and strains in agreement with gene sequence analyses (Mulet
et al., 2012; Scotta et al., 2013; Mulet et al., 2016; Mulet et al., 2017).
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From all these studies MALDI-TOF MS has been revealed as a powerful technique
for the identification of pathogenic species, nevertheless, this technology can be
applied to any bacteria if the databases are enlarged with the spectra of bacteria from
other origins (Rahi et al., 2016). Currently environmental species of Pseudomonas
have been also identified by using this methodology, some of them isolated from
water (Emami et al., 2012) or roots of cereals (Stets et al., 2013). In addition this
methodology has been used for new species description in the present decade, such as
P. arsenicoxydans (Campos et al., 2010), P. entomophila (Mulet et al., 2012), P.
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prosekii (Kosina et al., 2013), P. alkylphenolica (Mulet et al., 2015), P. kribbensis

(Chang et al., 2016) and P. cerasi (Kałużna et al., 2016).
5. Conclusions
At present we have a plethora of methodologies and techniques that allow the
differentiation of bacterial genera and species. These modern procedures led to an
explosive increase in the number of taxa described annually, contributing also to
wider biodiversity studies. Moreover, the current generalized sequencing of complete
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bacterial genomes has significantly increased the level of knowledge in Bacteriology.
In the case of genus Pseudomonas, more than 70 novel species have been described
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since 2009, with an annual average of 10 new species in the last three years. Since
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most of the environments in which Pseudomonas strains may be present remain
unexplored, it is foreseeable that the number of species of Pseudomonas will increase
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enormously in the next years. This fact, together with the phylogenetic complexity of
this genus, will likely force it to be splitted in more genera.
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Acknowledgments
The authors would like to thank our numerous collaborators and students involved in
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this research over the years. Funding was provided by Ministerio de Economía,
Industria y Competitividad (MINECO) and Junta de Castilla y León from Spain.
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Figure legends
Figure 1. Phylogenetic tree showing the phylogenetic positions of the recently

described species from genus Pseudomonas based on the analysis of the complete
sequences of the 16S rRNA gene. Distance was calculated by the Kimura‟s two-
parameter model. Phylogenetic tree was generated by neighbour-joining. The
significance of each branch is indicated by a bootstrap value (in percentage)
calculated for 1000 subsets (only values higher than 50% are indicated). Bar, 1
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substitution per 100 nucleotide positions.
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Figure 2. MLSA phylogenetic tree showing the clustering of the recently described
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species from genus Pseudomonas in the previously defined phylogroups based on the
analysis of concatenated 16S rRNA, gyrB, rpoB and rpoD genes. Distance was
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calculated by Jukes-Cantor model. Phylogenetic tree was generated by neighbour-
joining. The significance of each branch is indicated by a bootstrap value (in
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percentage) calculated for 1000 subsets (only values higher than 50% are indicated).
Bar, 5 substitution per 100 nucleotide positions. In the figure the groups and
phylogenetic lineages proposed by Mulet et al. (2010) and García-Valdés and Lalucat
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(2016) are indicated.

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Table 1. New species of genus Pseudomonas described since year 2009
Species Isolation source of type strain Geographic location Reference

Pseudomonas tuomuerensis* bird‟s nest China Xin et al. (2009)
Pseudomonas sabulinigri
Pseudomonas xinjiangensis
black beach sand
desert sand
Jeju Island, Korea
China
P T Kim et al. (2009)

Liu et al. (2009)
Pseudomonas cuatrocienegasensis
Pseudomonas caeni
Pseudomonas extremaustralis
evaporating lagoon
anaerobic ammonium-oxidizing bioreactor
temporary pond
Mexico
China
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Antarctica
I Escalante et al. (2009)
Xiao et al. (2009)
López et al. (2009)
Pseudomonas pelagia
Pseudomonas benzenivorans
Pseudomonas saponiphila
the Antarctic green alga Pyramimonas gelidicola
contaminated groundwater from an industrial plant site
no available data
C
Antarctica
S
USA
USA
Hwang et al. (2009)
Lang et al. (2010)
Lang et al. (2010)
Pseudomonas arsenicoxydans
Pseudomonas taiwanensis
sediment samples
soil
N U Chile
Taiwan
Campos et al. (2010)
Wang et al. (2010)
Pseudomonas taeanensis
Pseudomonas batumici
Pseudomonas seleniipraecipitatus
Pseudomonas protegens
crude oil-contaminated seashore
soil coast
soil
M A
soil suppressing black root rot of tobacco (Nicotiana glutinosa)
Korea
Caucasus, Black Sea
USA
Switzerland
Lee et al. (2010)
Kiprianova et al. (2011)
Hunter et al. (2011)
Ramette et al. (2011)
Pseudomonas toyotomiensis
Pseudomonas bauzanensis soil
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soil immersed in hot-spring water containing hydrocarbons Japan
Italy
Hirota et al. (2011)
Zhang et al. (2011)
Pseudomonas deceptionensis
Pseudomonas composti
Pseudomonas litoralis
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marine sediment sample collected
compost samples from vegetable and animal waste
Mediterranean seawater
Deception Island, Antarctica
Spain
Spain
Carrión et al. (2011)
Gibello et al. (2011)
Pascual et al. (2012)
Pseudomonas baetica
Pseudomonas entomophila
Pseudomonas kuykendallii C E
wedge sole, Dicologlossa cuneata (Moreau)
female specimen of Drosophila melanogaster
hexazinone degrading bioreactor
Spain
Guadeloupe Island, Mexico
USA
López et al. (2012)
Mulet et al. (2012a)
Hunter and Manter (2012)
Pseudomonas nitritireducens
Pseudomonas zeshuii
Pseudomonas linyingensis A C
wheat soil subjected to long-term herbicides application
herbicide-contaminated soil
wheat soil subjected to long-term herbicides application
China
China
China
Wang et al. (2012)
Feng et al. (2012)
He et al. (2012)
Pseudomonas punonensis straw grass Peru Ramos et al. (2013)
Pseudomonas asturiensis soybean and weeds Spain González et al. (2013)
Pseudomonas sagittaria oil-contaminated soil Taiwan Lin et al. (2013a)
Pseudomonas formosensis food-waste compost Taiwan Lin et al. (2013b)
Pseudomonas guariconensis rhizospheric soil of Vigna unguiculata (L.) Walp. Venezuela Toro et al. (2013)
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Pseudomonas guguanensis hot spring sample Taiwan Liu et al. (2013)

Pseudomonas guangdongensis electroactive biofilm China Yang et al. (2013)
Pseudomonas prosekii soil James Ross Island, Antarctica Kosina et al. (2013)
Pseudomonas oryzae paddy soil China Yu et al. (2013)
Pseudomonas yangmingensis hot spring Taiwan Wong and Lee (2014)
Pseudomonas chengduensis landfill leachate in a solid-waste disposal site China
P T Tao et al. (2014)

Pseudomonas kunmingensis
Pseudomonas aestusnigri
Pseudomonas sihuiensis
phosphate mine
crude oil-contaminated intertidal sand samples
forest soil
China
Spain
China
R I Xie et al. (2014)
Sánchez et al. (2014)
Wu et al. (2014)
Pseudomonas helmanticensis
Pseudomonas hussainii
Pseudomonas hunanensis
forest soil
droppings of a seashore bird
soil subjected to long-term manganese pollution
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Spain
Taiwan
China
Ramírez-Bahena et al. (2014)
Hameed et al. (2014)
Gao et al. (2014)
Pseudomonas soli
Pseudomonas salegens
Pseudomonas asuensis
soil sample from Sierra Nevada Park
aquatic plants of the Gomishan wetland
biological soil crusts
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Iran
USA
Amoozegar et al. (2014)
Reddy et al. (2015)
Pseudomonas donghuensis
Pseudomonas yamanorum
Pseudomonas granadensis
water of East Lake
soil samples
soil from Almijara and Alhama Natural Park M A China
Isla de los Estados, Argentina
Spain
Gao et al. (2015)
Arnau et al. (2015)
Pseudomonas matsuisoli
Pseudomonas songnenensis
Pseudomonas zhaodongensis
soil sample
saline and alkaline soils
saline and alkaline soils
E D Matsu Island, Taiwan
China
China
Lin et al. (2015)
Zhang et al. (2015a)
Zhang et al. (2015b)
Pseudomonas glareae
Pseudomonas endophytica
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sediment sample collected from the sea
stem tissue of Solanum tuberosum L.
Japan
Spain
Romanenko et al. (2015)
Ramírez-Bahena et al. (2015)
Pseudomonas salina
Pseudomonas coleopterorum
Pseudomonas alkylphenolica soil
C E
salt lake Xiaochaidan
the bark beetle Hylesinus fraxini
China
Czech Republic
South Korea
Zhong et al. (2015)
Menéndez et al. (2015)
Mulet et al. (2015)
Pseudomonas flexibilis
Pseudomonas populi
Pseudomonas helleri A C
pond water-mud slurry
stems of Populus euphratica trees
raw cow's milk
USA
China
Germany
Hespell, 1977
Anwar et al. (2016)
von Neubeck et al. (2016)
Pseudomonas weihenstephanensis raw cow's milk Germany von Neubeck et al. (2016)
„Pseudomonas gregormendelii‟ mineral substrate James Ross Island, Antarctica Kosina et al. (2016)
Pseudomonas cerasi diseased tissue of cherry Poland Kałużna et al. (2016)
Pseudomonas oceani deep seawater Northwestern Pacific Ocean Wang and Sun (2016)
Pseudomonas turukhanskensis oil-contaminated soils East Siberia, Russia Korshunova et al. (2016)
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Pseudomonas kribbensis garden soils Korea Chang et al. (2016)

Pseudomonas canadensis a field plot under long-term mineral fertilization Canada Tambong et al. (2016)
‘Pseudomonas saudiphocaensis’ currency notes collected during the Hajj pilgrimage Saudi Arabia Azhar et al. (2016)
'Pseudomonas saudimassiliensis' air samples in an urban environment Saudi Arabia Azhar et al. (2017)
Pseudomonas lactis bovine raw milk Germany von Neubeck et al. (2017)
Pseudomonas paralactis bovine raw milk Germany
P T von Neubeck et al. (2017)

„Pseudomonas sesami‟
Pseudomonas versuta
Pseudomonas caspiana
rhizosphere of Sesamum indicum L.
soil
leaves and stems of citrus
Nigeria
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Lagoon Island, Antarctica
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Northern Iran
Madhaiyan et al. (2017)
See-Too et al. (2017)
Busquets et al. (2017)
‘Pseudomonas massiliensis‟
Pseudomonas aestus
Pseudomonas reidholzensis
stools
mangrove sediments
forest soil
S C Brazil
Brazil
Switzerland
Bardet et al. (2017)
Vasconcellos et al. (2017)
Frasson et al. (2017)
Pseudomonas wadenswilerensis
Pseudomonas tarimensis
forest soil
stems of Populus euphratica
N U Switzerland
China
Frasson et al. (2017)
Anwar et al. (2017)
This species has been proposed to be a later heterotypic synonym of Pseudomonas fexibilis (Shin et al., 2015) which was validated in IJSEM (Validation list 168).
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Table 2. Type strains of Pseudomonas species from which the complete genome is available in
different databases
Type strains Accession numbers

P. abietaniphila ATCC 700689, LMG 20220 GCF_900100795.1, Gp0127165
P. aeruginosa DSM 50071 GCF_001045685.1, Gp0120920
P. aeruginosa NCTC 10332 Gp0132017
P. agarici NCPPB 2289 GCF_000280785.1, Gp0005914
P. alcaligenes NBRC 14159 GCF_000467105.1, Gp0024155
P. alcaliphila JCM 10630, NBRC 102411 GCF_900101755.1, Gp0023992
P. alkylphenolica KL28 GCF_000746525.1
P. amygdali CFBP 3205 GCF_000935645.1
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P. antarctica DSM 15318 Gp0008489
P. argentinensis LMG 22563 Gp0127182
P. asplenii LMG 2137 Gp0127166
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P. avellanae IC 631 GCF_000302915.1, Gp0020557
P. azotifigens DSM 17556, DSM 17556 GCF_000425625.1, Gp0022639
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P. azotoformans LMG 21611, NBRC 12693 GCF_001870415.1, Gp0024156
P. baetica LMG 25716 Gp0112912
P. balearica DSM 6083 GCF_000818015.1, Gp0118173
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P. batumici UCM B-321 GCF_000820515.1
P. bauzanensis DSM 22558, LMG 26048 GCF_900111225.1, Gp0127174
P. benzenivorans DSM 8628 Gp0127187
P. borbori LMG 23199 Gp0127162
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P. caeni DSM 24390 GCF_000421765.1, Gp0013191

P. canadensis 2-92 GCF_000503215.1
P. cannabina ICMP 2823, CFBP 2341 Gp0146366, Gp0127163
P. caspiana FBF102 GCF_000802425.1
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P. cerasi 58 GCF_900074915.1
P. chloritidismutans AW-1 Gp0047675
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P. chlororaphis subsp. aureofaciens LMG 1245, NBRC 3521 GCF_001269575.1, Gp0023849

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P. chlororaphis subsp. chlororaphis NBRC 3904 Gp0023850

P. chlororaphis subsp. piscium DSM 21509 GCF_001269555.1
P. cichorii ATCC 10857, NCPPB 943 GCF_900104015.1, Gp0127167
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P. citronellolis NBRC 103043 Gp0024157

P. composti CCUG 59231, CECT 7516 GCF_900115475.1, Gp0127176
P. congelans DSM 14939, LMG 21466 GCF_900103225.1, Gp0127158
P. coronafaciens ICMP 8921 GCF_001401235.1
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P. cremoricolorata DSM 17059, NBRC 16634, DSM 17059 GCF_000425745.1

P. cuatrocienegasensis LMG 24676 Gp0127173
P. deceptionensis DSM 26521, LMG 25555 GCA_001042895.1, Gp0120258
P. delhiensis CCM 7361, LMG 24737 GCA_900099945.1, Gp0127157
P. donghuensis HYS GCF_000259195.1
P. duriflava CGMCC 1.6858 Gp0093941
P. endophytica BSTT44 GCF_001411475.1
P. entomophila L48 GCF_000026105.1, Gp0000348
P. extremaustralis DSM 17835 GCF_900102035.1, Gp0120259
P. flavescens NBRC 103044 Gp0014249
P. flexibilis CGMCC 1.1365, ATCC 29606, JCM 14085 GCF_900101515.1, Gp0127303, Gp0118199
P. fluorescens DSM 50090, NBRC 14160 GCF_001269845.1, Gp0018925
P. fragi NRRL B-727, NBRC 3458 GCF_900105835.1, Gp0023846
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P. fulva NBRC 16637, DSM 17717, NBRC 16637 GCF_000621265.1, Gp0039998, Gp0023554
P. fuscovaginae ICMP 5940 GCF_000467065.1, Gp0049954
P. graminis DSM 11363, LMG 21661 GCA_900111735.1, Gp0127164
P. guineae LMG 24016 Gp0127186
P. helleri DSM 29165 GCA_001043025.1
P. hibiscicola ATCC 19867 GCF_000382065.1
P. hussainii JCM 19513 GCF_900109735.1
P. indica NBRC 103045 Gp0024159
P. japonica NBRC 103040, DSM 22348, NBRC 103040 GCF_000730585.1, Gp0148719
P. jinjuensis NBRC 103047 Gp0024161
P. kilonensis DSM 13647 GCF_001269885.1, Gp0145008
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P. knackmussii B13 GCF_000689415.1
P. kuykendallii LMG 26364 Gp0127179
P. litoralis CECT 7670 Gp0127175
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P. lundensis DSM 6252 GCA_001042985.1
P. lutea DSM 17257, LMG 21974 GCF_000759445.1, Gp0131761
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P. luteola NBRC 103146 Gp0024000
P. mandelii NBRC 103147 Gp0023851
P. marincola LMG 24752 Gp0127170
P. massiliensis CB-1 GCF_000826105.1
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P. mediterranea DSM 16733, CFBP 5447 GCF_900106005.1, Gp0102154
P. mendocina NBRC 14162 GCF_000813265.1, Gp0024092
P. migulae NBRC 103157 Gp0024162
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P. mohnii DSM 18327 Gp0127185

P. monteilii NBRC 103158 GCF_000730605.1, Gp0023814
P. mosselii DSM 17497 GCF_000621225.1, Gp0039999
P. mucidolens NBRC 103159 Gp0024204
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P. nitroreducens NBRC 12694 Gp0024205

P. oleovorans LMG 2229 Gp0127178
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P. oleovorans subsp. oleovorans NBRC 13583 Gp0023843

P. orientalis DSM 17489 GCF_001439815.1
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P. oryzihabitans NBRC 102199 GCF_000730625.1, Gp0024206

P. otitidis DSM 17224, LMG 23769 GCF_900111835.1, Gp0127161
P. pachastrellae LMG 23570 Gp0127160
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P. panipatensis CCM 7469, LMG 24738 GCA_900099785.1, Gp0127172

P. parafulva NBRC 16636, DSM 17004 GCF_000730645.1, Gp0024207, Gp0021954
P. pelagia CL-AP6 GCF_000410875.1, Gp0041739
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P. peli LMG 23201 Gp0127168

P. pertucinogena DSM 18268 Gp0013192
P. pictorum JCM 9942 GCF_001310775.1
P. plecoglossicida NBRC 103162 GCF_000730665.1, Gp0024208
P. poae DSM 14936, DSM 14936 GCF_001439785.1, Gp0133356
P. pohangensis DSM 17875 Gp0127183
P. protegens CHA0 GCF_000397205.1
P. pseudoalcaligenes NBRC 14167 Gp0023768
P. psychrotolerans DSM 15758, LMG 21977 GCF_900102665.1, Gp0127177
P. punonensis CECT 8089, LMG 26839 GCF_900142655.1, Gp0127180
P. putida NBRC 14164 GCF_000412675.1
P. resinovorans DSM 21078 GCF_000423545.1, Gp0013193
P. rhizosphaerae DSM 16299 GCF_000761155.1
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P. sabulinigri CECT 7679 Gp0127171

P. salomonii LMG 22120 Gp0127155
P. saponiphila DSM 9751 Gp0127188
P. segetis DSM 18913 Gp0127159
P. seleniipraecipitatus LMG 25475 Gp0131762
P. simiae CCUG 50988, DSM 18861 GCF_900111895.1, Gp0127156
P. straminea NBRC 16665 Gp0024209
P. stutzeri CGMCC 1.1803, ATCC 14405 GCF_000219605.1, Gp0011553, Gp0016674, Gp0011322
P. synxantha DSM 18928, NBRC 3913 GCF_001439725.1, Gp0023772
P. syringae KCTC 12500 GCF_000507185.2
P. taeanensis MS-3 GCF_000498575.2, Gp0049072
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P. taetrolens DSM 21104 GCA_001042915.1
P. taiwanensis DSM 21245, DSM 21245 GCF_000425785.1, Gp0118198
P. thermotolerans DSM 14292 GCF_000364625.1, Gp0013194
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P. thivervalensis DSM 13194 GCF_001269655.1
P. tolaasii NCPPB 2192 Gp0112886
P. toyotomiensis JCM 15604 GCF_900115695.1, Gp0127184
SC
P. tremae CFBP 3225 GCF_000935675.1
P. trivialis DSM 14937 GCF_001439805.1, Gp0133357
P. tuomuerensis JCM 14085 GCF_000806415.1
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P. veronii DSM 11331 GCF_001439695.1
P. versuta L10.10 Gp0124606
P. viridiflava DSM 6694 GCF_001305955.1
MA
P. vranovensis DSM 16006 GCF_000425805.1, Gp0021956

P. weihenstephanensis DSM 29166 GCA_001043055.1
P. xanthomarina DSM 18231 GCF_900129835.1, Gp0040001
P. xiamenensis DSM 22326 Gp0013197
P. xinjiangensis CCTCC 207151 Gp0127169
D
P. zeshuii KACC 15471, DSM 27927 GCF_900141925.1, Gp0127181

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Fig. 1
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Fig. 2
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Highlights:
- The Pseudomonas taxonomy continues progressing very active, with the

description of more than 70 novel species in the last years
- The analysis of complete genomes has proven very useful in the taxonomy
of genus Pseudomonas, leading also to a better knowledge of the biology of
their species
- The diverse habitats in which the recently described species of
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Pseudomonas have been found and their biological abilities confirmed their
enormous metabolic versatility.
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The Current Status On The Taxonomy of Pseudomonas Revisited, Peix2018

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The current status on the taxonomy of Pseudomonas revisited: An

Alvaro Peix, Martha-Helena Ramírez-Bahena, Encarna Velázquez

The current status on the taxonomy of Pseudomonas revisited: an update

Alvaro Peix1,2, Martha-Helena Ramírez-Bahena3 and Encarna Velázquez2,3

1. Instituto de Recursos Naturales y Agrobiología. IRNASA-CSIC. Salamanca.

Running title: Pseudomonas taxonomy

Keywords: Pseudomonas; taxonomy; MLSA; genomes; MALDI-TOF MS

1. The genus Pseudomonas: a brief historical review

rRNA subgroups based on the measurements of RNA-DNA and this classification

classification of bacteria placing the genus Pseudomonas into the Gamma

2. The recently described species: from 2009 onwards

Gao et al., 2015), P. guariconensis and P. helmanticensis, could solubilize phosphate

several PGPR mechanisms and P. protegens and P. canadensis, were reported as

3. Current methods used in Pseudomonas taxonomy

Pseudomonas species (Palleroni, 2015).

studies. Although fingerprinting techniques such as amplified ribosomal DNA

enterobacterial repetitive intergenic consensus (ERIC), bacterial repetitive BOX

Kallufa et al., 2017; Rijaveca and Lapanje, 2017).

and a MLSA (multilocus sequence analysis) database (PseudoMLSA) has been

2015; García-Valdés and Lalucat, 2016). According to these authors, the P.

P. fluorescens group, which includes numerous subgroups. The P. aeruginosa lineage

groups, such as P. turukhanskensis, P. massiliensis, P. kuykendallii, P. salegens and

(http://www.bacterio.net/pseudomonas.html). It is likely that in the future the current

and chemotaxonomic analyses, if a thorough taxonomic revision of family

4. Modern approaches in Pseudomonas taxonomy: the omics era

comparison and analysis of whole genomes is a good tool in Pseudomonas taxonomy

have been analysed in recently published descriptions of new species, such as P.

DNA-DNA hybridization classically established for experimental laboratory

comparable to the results of automatized phenotypic methods (Jamal et al., 2014).

prosekii (Kosina et al., 2013), P. alkylphenolica (Mulet et al., 2015), P. kribbensis

Amoozegar, M.A., Shahinpei, A., Sepahy, A.A., Makhdoumi-Kakhki, A.,

Culturable bacterial populations associated with ectomycorrhizae of Norway spruce

'Pseudomonas saudiphocaensis' sp. nov., a new bacterial species isolated from

M.A., López-López, A., Rosselló-Móra, R., 2010. Pseudomonas arsenicoxydans sp.

Chao, J., Wolfaardt, G.M., Arts, M.T., 2010. Characterization of Pseudomonas

bacterial gall on Loropetalum chinense caused by Pseudomonas savastanoi in the

United States. Plant Dis. 97, 835.

composition and Adansonian analysis of heterotrophic aerobic pseudomonads. J.

MALDI-TOF mass spectrometry. PLoS One 7, e38515.

Escalante, A.E., Caballero-Mellado, J., Martínez-Aguilar, L., Rodríguez-Verdugo, A.,

González-González, A., Toribio-Jiménez, J., Souza, V., 2009. Pseudomonas

cuatrocienegasensis sp. nov., isolated from an evaporating lagoon in the Cuatro

Rd. Science. 269, 496–512.

U., 2017. Pseudomonas wadenswilerensis sp. nov. and Pseudomonas reidholzensis

soil. Int. J. Syst. Evol. Microbiol. 67:.2853-2861.

and systematics in Pseudomonas. Front. Microbiol. 6, 214.

González, A.J., Cleenwerck, I., De Vos, P., Fernández-Sanz, A.M., 2013.

Microbiol. 36, 320–324.

erecta) caused by Pseudomonas cichorii and a Xanthomonas species in Florida. Plant

Hunter, W.J., Manter, D.K., 2011. Pseudomonas seleniipraecipitatus sp. nov.: a

proteobacteria isolated from a hexazinone degrading bioreactor. Curr. Microbiol. 65,

desorption-ionization time-of-flight mass spectrometry systems, for identification of

Johnson, J. L., Palleroni, N., 1989. Deoxyribonucleic acid similarities among

of cherry. Syst. Appl. Microbiol. 39, 370–377.

in Parana, Brazil. Infect. Genet. Evol. 49, 130–133.

at a cystic fibrosis centre. J. Hosp. Infect. 92, 54–60.

Keshtkar, A.R., Khodakaramian, G., Rouhrazi, K., 2016. Isolation and