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Review Article

Probiotics in aquaculture

Priyadarshini Pandiyan a,*, Deivasigamani Balaraman b, Rajasekar Thirunavukkarasu a,

Edward Gnana Jothi George a, Kumaran Subaramaniyan a, Sakthivel Manikkam a,
Balamurugan Sadayappan a
a
Ph.D Research Scholar, CAS in Marine Biology, Annamalai University, Parangipettai 608502, Tamil Nadu, India
b
Assistant Professor, CAS in Marine Biology, Annamalai University, Parangipettai 608502, Tamil Nadu, India

article info abstract

Article history: Aquaculture is the world’s fastest growing food production sector. However, fish culture is
Received 10 January 2013 currently suffering from serious losses due to infectious diseases. The use of antimicrobial
Accepted 8 March 2013 drugs, pesticides and disinfectant in aquaculture disease prevention and growth promo-
tion has led to the evolution of resistant strains of bacteria. Thus, the research into the use
of probiotics for aquaculture is increasing with the demand for environment e friendly
Keywords: sustainable aquaculture. The benefits of such supplements include improved feed value,
Probiotic enzymatic contribution to digestion, inhibition of pathogenic microorganisms, anti-
Aquaculture mutagenic and anti-carcinogenic activity, and increased immune response. These pro-
Lactic acid bacteria biotics are harmless bacteria that help the well being of the host animal and contribute,
Bacillus sp directly or indirectly to protect the host animal against harmful bacterial pathogens. The
use of probiotics in aquaculture has just begun, due to the fact that gastrointestinal
microbiota of aquatic organisms has been poorly characterized, and their effects are not
studied extensively. This review summarizes and evaluates brief knowledge about the
probiotic organism, the action of probiotic in fish culture and the safety evaluation of
probiotics in aquaculture.
Copyright ª 2013, JPR Solutions; Published by Reed Elsevier India Pvt. Ltd. All rights
reserved.

1. Introduction During the last decades, antibiotics used as traditional

strategy for fish diseases management and also for the
Today, aquaculture is the fastest growing food-producing improvement of growth and efficiency of feed conversion.
sector in the world, with an average annual growth rate of However, the development and spread of antimicrobial resis-
8.9% since 1970, compared to only 1.2% for capture fisheries tant pathogens were well documented.3,4 There is a risk asso-
and 2.8% for terrestrial farmed meat production systems over ciated with the transmission of resistant bacteria from
the same period.1 World aquaculture has grown tremen- aquaculture environments to humans, and risk associated
dously during the last fifty years from a production of less with the introduction in the human environment of non-
than a million tonne in the early 1950s to 59.4 million tonnes pathogenic bacteria, containing antimicrobial resistance
by 2004. This level of production had a value of US$70.3 billion. genes, and the subsequent transfer of such genes to human
The diseases and deterioration of environmental conditions pathogens.5 Considering these factors, there has been height-
often occur and result in serious economic losses.2 ened research in developing new dietary supplementation

* Corresponding author. Tel.: þ91 9524149006.

E-mail address: priyadarshinibio87@gmail.com (P. Pandiyan).
0975-7619/$ e see front matter Copyright ª 2013, JPR Solutions; Published by Reed Elsevier India Pvt. Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.dit.2013.03.003
56 d r u g i n v e n t i o n t o d a y 5 ( 2 0 1 3 ) 5 5 e5 9

strategies in which various health and growth promoting and food ingredients and such actions may result in inactivation
compounds as probiotics, prebiotics, synbiotics, phytobiotics of toxins and detoxification of host and food components in the
and other functional dietary supplements have been evalu- gut. According to above summary, all three modes of probiotics
ated.6 In this context, microbial intervention can play a vital actions are all likelihood associated with gut and/or gut
role in aquaculture production, and effective probiotic treat- microbiota. Therefore, it has become apparent that we are in fact
ments may provide broad spectrum and greater nonspecific dealing with another “organ”, the so called “microbiotic canal”
disease protection.7,8 This review summarizes and evaluates with the increased knowledge of the specific activity of the gut
the broader knowledge about the probiotics, selection of pro- microbiota.17
bionts, commonly used probiotic organism, their mode of ac-
tion and safety regulation of probiotics in aquaculture.
4. Probiotic organism

2. Definition of probiotics Today probiotics are quite commonplace in health promoting

“functional foods” for humans, as well as therapeutic, pro-
The word “probiotic” was introduced by Parker, 1974.9 Ac- phylactic and growth supplements in animal production and
cording to his original definition, probiotics are “organisms human health.18e20 Typically, the lactic acid bacteria (LAB)
and substances which contribute to intestinal microbial bal- have been widely used and researched for human and
ance”. Fuller, 198910 revised the definition as “live microbial terrestrial animal purposes, and LAB are also known to be
feed supplement which beneficially affects the host animal by present in the intestine of healthy fish.21,22 Interest in LAB
improving its intestinal microbial balance”. Therefore, several stems from the fact that they are natural residents of the
terms such as “friendly”, “beneficial”, or “healthy” bacteria are human GIT with the ability to tolerate the acidic and bile
also commonly used to describe probiotics. Although appli- environment of the intestinal tract. LAB also function to
cation of probiotics in aquaculture seems to be relatively convert lactose into lactic acid, thereby reducing the pH in the
recent,11 the interest in such environment friendly treatments GIT and naturally preventing the colonization by many bac-
is increasing rapidly. Moriarty, 199812 proposed to extend the teria,23 The most widely researched and used lactic acid bac-
definition of probiotics in aquaculture to microbial ‘‘water teria are the Lactobacilli and Bifidobacteria.20,24,25
additives’’. A growing number of studies have dealt explicitly Other commonly studied probiotics include the spore form-
with probiotics, and it is now possible to survey its state of the ing Bacillus sp. and yeasts. Bacillus sp. have been shown to possess
art, from the empirical use to the scientific approach.13,14 adhesion abilities, produce bacteriocins (antimicrobial peptides)
and provide immunostimulation.26e29 Gram-positive obligate or
facultative anaerobes are dominant in the gastrointestinal
3. Selection of probiotics microbiota of man and terrestrial farm animals.30 Most probionts
belong to dominant or sub-dominant genera among these
Selection of probiotic bacteria has usually been an empirical microbiota, e.g., Bifidobacterium, Lactobacillus, Streptococcus.30
process based on limited scientific evidence. Many of the Gram-negative facultative anaerobes prevail in the digestive
failures in probiotic research can be attributed to the selection tract of fish and shellfish, though symbiotic anaerobes may be
of inappropriate microorganisms. Selection steps have been dominant in the posterior intestine of some herbivorous tropical
defined, but they need to be adapted for different host species fish.31 Vibrio and Pseudomonas are the most common genera in
and environments. It is essential to understand the mecha- crustaceans,32 marine fish and bivalves.33,34 Aeromonas, Plesio-
nisms of probiotic action and to define selection criteria for monas and Enterobacteriaceae are dominant in freshwater fish.33
potential probiotics.15 General selection criteria are mainly Bacillus spp. hold added interest in probiotics as they can be
determined by bio safety considerations, kept in the spore form and therefore stored indefinitely on the
shelf.35 The list of microorganism authorized as probiotics in
a. Methods of production and processing. feeding stuffs under Council Directive 70/524/EEC are given in
b. Method of administration of the probiotic and Table 1. In addition, other probiotics are commercialized on the
c. The location in the body where the microorganisms are market that has been notified, but that do not appear in the last
expected to be active.15 authorized list of feed additives published by the Commission.

Three general modes of probiotics actions have been classi-

fied and presented by Oelschlaeger, 201016 as follow: (1) Pro- 5. Mechanisms of action
biotics might be able to modulate the host’s gut defenses
including the innate as well as the acquired immune system and Different modes of action or properties are desire on the po-
this mode of action is most likely important for the prevention tential probiotic like antagonism to pathogens36,37 ability of cells
and therapy of infectious diseases but also for the treatment of to produce metabolites (like vitamins) and enzymes,38 coloni-
inflammation of the digestive tract or parts thereof. (2) Probiotics zation or adhesion properties39 enhance the immune system.40
can also have a direct effect on other organisms, commensal and
or pathogenic ones and this principle is in many cases is of great 5.1. Competitive exclusion of pathogenic bacteria
importance in the prevention, treatment and restoration of the
microbial equilibrium in the gut. (3) Finally, probiotic effects may Competitive exclusion is a phenomenon whereby an estab-
be based on actions affecting microbial products, host products lished microflora prevents or reduces the colonization of a
 d r u g i n v e n t i o n t o d a y 5 ( 2 0 1 3 ) 5 5 e5 9 57

natural or nonspecific defense system formed by a series of

Table 1 e List of microorganism authorized as probiotics
in feeding stuffs under Council Directive 70/524/EEC. cellular and humoral components, and 2) the adaptive, ac-
quired or specific immune system characterized by the hu-
S. no. Probiotic organism
moral immune response through the production of antibodies
1. Bacillus cereus var. toyoi and by the cellular immune response which is mediated by T-
2. Bacillus licheniformis lymphocytes, capable of reacting specifically with antigens.
3. Bacillus subtilis
The normal microbiota in the GI ecosystem influences the
4. Enterococcus faecium
innate immune system, which is of vital importance for the
5. Lactobacillus casei
6. Lactobacillus farciminis disease resistance of fish and is divided into physical barriers,
7. Lactobacillus plantarum humoral and cellular components. Innate humoral parame-
8. Lactobacillus rhamnosus ters include antimicrobial peptides, lysozyme, complement
9. Pediococcus acidilactici components, transferring, pentraxins, lectins, antiproteases
10. Saccharomyces cerevisiae and natural antibodies, whereas nonspecific cytotoxic cells
11. Streptococcus infantarius
and phagocytes constitute innate cellular immune effectors.
Cytokines are an integral component of the adaptive and
competing bacterial challenge for the same location on the innate immune response, particularly IL-1b, interferon, tumor
intestine. The aim of probiotic products designed under necrosis factor-a, transforming growth factor-b and several
competitive exclusion is to obtain: stable, agreeable and cehmokines regulate innate immunity.44 The nonspecific
controlled microbiota in cultures based on the following; immune system can be stimulated by probiotics. It has been
competition for attachment sites on the mucosa, competition demonstrated that oral administration of Clostridium butyr-
for nutrients and production of inhibitory substances by the icum bacteria to rainbow trout enhanced the resistance of fish
microflora which prevents replication and/destroys the chal- to vibriosis, by increasing the phagocytic activity of leuco-
lenging bacteria and hence reduce colonization.12 Different cytes. Rengpipat et al, 20007 mentioned that the use of Bacillus
strategies are displayed in the adhesion of microorganism to sp. (strain S11) provided disease protection by activating both
those attachment sites as passive forces, electrostatic in- cellular and humoral immune defenses in tiger shrimp
teractions, hydrophobic, steric forces, lipoteichoic acids, ad- (Penaeus monodon). Balcazar, 200345 demonstrated that the
hesions and specific structures of adhesion.41Adhesion and administration of a mixture of bacterial strains (Bacillus and
colonization of the mucosal surfaces are possible protective Vibrio sp.) positively influenced the growth and survival of
mechanisms against pathogens through competition for juveniles of white shrimp and presented a protective effect
binding sites and nutrients.42 against the immune system, by increasing phagocytosis and
antibacterial activity.
5.2. Production of inhibitory compounds
5.4. Antiviral effects
Bacterial antagonism is a common phenomenon in nature;
therefore, microbial interactions play a major role in the equi- Some bacteria used as candidate probiotics have antiviral ef-
librium between competing beneficial and potentially patho- fects. Although the exact mechanism by which these bacteria
genic microorganisms.43 Antagonistic compounds are defined exerts its antiviral effects is not known, laboratory tests in-
as chemical substances produced by microorganisms (in this dicates that the inactivation of viruses can occur by chemical
case bacteria) that are toxic (bactericidal) or inhibitory (bacte- and biological substances, such as extracts from marine algae
riostatic) toward other microorganisms. The presence of bacte- and extracellular agents of bacteria. It has been reported that
ria producing antibacterial compounds in the intestine of the strains of Pseudomonas sp., Vibrio sp., Aeromonas sp., and
host, on its surface, or in its culture water is thought to prevent groups of coryneforms isolated from salmonid hatcheries,
proliferation of pathogenic bacteria and even eliminate these. showed antiviral activity against infectious hematopoietic
The structure of the antibacterial compound is often not eluci- necrosis virus (IHNV) with more than 50% plaque reduction.46
dated and their mode of action has not been reported. Further- Girones et al, 198947 reported that a marine bacterium,
more none of these reports demonstrate that the antibacterial tentatively classified in the genus Moraxella, showed antiviral
compound is produced in vivo. This will be of significant activity against poliovirus. Direkbusarakim et al, 199848 iso-
importance, if production of these compounds and its mode of lated two strains of Vibrio spp. from a black tiger shrimp
action are understood. If the production of antibacterial com- hatchery. These isolates displayed antiviral activities against
pound is the only mode of action, it is possible that the pathogen IHNV and Oncorhynchus masou virus (OMV), with percentages
eventually will develop resistance toward the compound. This of plaque reduction between 62 and 99%, respectively.
will result in an ineffective treatment. The risk of the pathogen to
develop resistance against the active compound has to be eval-
uated, to assure a stable effect of the probiotic bacterium. 6. Safety regulation

5.3. Enhancement of the immune response against The safety profile of a potential probiotic strain is of critical
pathogenic microorganisms importance in the selection process. This testing should
include the determination of strain resistance to a wide vari-
The immune systems of fish and higher vertebrates are ety of common classes of antibiotics such as tetracyclines,
similar and both have two integral components: 1) the innate, quinolones and macrolides and subsequent confirmation of
58 d r u g i n v e n t i o n t o d a y 5 ( 2 0 1 3 ) 5 5 e5 9

non-transmission of drug resistance genes or virulence plas- references

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