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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 b

Ph.D Research Scholar, CAS in Marine Biology, Annamalai University, Parangipettai 608502, Tamil Nadu, India Assistant Professor, CAS in Marine Biology, Annamalai University, Parangipettai 608502, Tamil Nadu, India

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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 promotion 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

Today, aquaculture is the fastest growing food-producing sector in the world, with an average annual growth rate of 8.9% since 1970, compared to only 1.2% for capture fisheries and 2.8% for terrestrial farmed meat production systems over the same period.1 World aquaculture has grown tremendously during the last fifty years from a production of less than a million tonne in the early 1950s to 59.4 million tonnes by 2004. This level of production had a value of US$70.3 billion. The diseases and deterioration of environmental conditions often occur and result in serious economic losses.2

During the last decades, antibiotics used as traditional strategy for fish diseases management and also for the improvement of growth and efficiency of feed conversion. However, the development and spread of antimicrobial resistant pathogens were well documented.3,4 There is a risk associated with the transmission of resistant bacteria from aquaculture environments to humans, and risk associated with the introduction in the human environment of nonpathogenic bacteria, containing antimicrobial resistance genes, and the subsequent transfer of such genes to human pathogens.5 Considering these factors, there has been heightened research in developing new dietary supplementation

* Corresponding author. Tel.: þ91 9524149006. E-mail address: [email protected] (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

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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 compounds as probiotics, prebiotics, synbiotics, phytobiotics and other functional dietary supplements have been evaluated.6 In this context, microbial intervention can play a vital role in aquaculture production, and effective probiotic treatments may provide broad spectrum and greater nonspecific disease protection.7,8 This review summarizes and evaluates the broader knowledge about the probiotics, selection of probionts, commonly used probiotic organism, their mode of action and safety regulation of probiotics in aquaculture.

and food ingredients and such actions may result in inactivation of toxins and detoxification of host and food components in the gut. According to above summary, all three modes of probiotics actions are all likelihood associated with gut and/or gut microbiota. Therefore, it has become apparent that we are in fact dealing with another “organ”, the so called “microbiotic canal” with the increased knowledge of the specific activity of the gut microbiota.17

4. 2.

Definition of probiotics

The word “probiotic” was introduced by Parker, 1974.9 According to his original definition, probiotics are “organisms and substances which contribute to intestinal microbial balance”. Fuller, 198910 revised the definition as “live microbial feed supplement which beneficially affects the host animal by improving its intestinal microbial balance”. Therefore, several terms such as “friendly”, “beneficial”, or “healthy” bacteria are also commonly used to describe probiotics. Although application of probiotics in aquaculture seems to be relatively recent,11 the interest in such environment friendly treatments is increasing rapidly. Moriarty, 199812 proposed to extend the definition of probiotics in aquaculture to microbial ‘‘water additives’’. A growing number of studies have dealt explicitly with probiotics, and it is now possible to survey its state of the art, from the empirical use to the scientific approach.13,14

3.

Selection of probiotics

Selection of probiotic bacteria has usually been an empirical process based on limited scientific evidence. Many of the failures in probiotic research can be attributed to the selection of inappropriate microorganisms. Selection steps have been defined, but they need to be adapted for different host species and environments. It is essential to understand the mechanisms of probiotic action and to define selection criteria for potential probiotics.15 General selection criteria are mainly determined by bio safety considerations, a. Methods of production and processing. b. Method of administration of the probiotic and c. The location in the body where the microorganisms are expected to be active.15 Three general modes of probiotics actions have been classified and presented by Oelschlaeger, 201016 as follow: (1) Probiotics might be able to modulate the host’s gut defenses including the innate as well as the acquired immune system and this mode of action is most likely important for the prevention and therapy of infectious diseases but also for the treatment of inflammation of the digestive tract or parts thereof. (2) Probiotics can also have a direct effect on other organisms, commensal and or pathogenic ones and this principle is in many cases is of great importance in the prevention, treatment and restoration of the microbial equilibrium in the gut. (3) Finally, probiotic effects may be based on actions affecting microbial products, host products

Probiotic organism

Today probiotics are quite commonplace in health promoting “functional foods” for humans, as well as therapeutic, prophylactic and growth supplements in animal production and human health.18e20 Typically, the lactic acid bacteria (LAB) have been widely used and researched for human and terrestrial animal purposes, and LAB are also known to be present in the intestine of healthy fish.21,22 Interest in LAB stems from the fact that they are natural residents of the human GIT with the ability to tolerate the acidic and bile environment of the intestinal tract. LAB also function to convert lactose into lactic acid, thereby reducing the pH in the GIT and naturally preventing the colonization by many bacteria,23 The most widely researched and used lactic acid bacteria are the Lactobacilli and Bifidobacteria.20,24,25 Other commonly studied probiotics include the spore forming Bacillus sp. and yeasts. Bacillus sp. have been shown to possess adhesion abilities, produce bacteriocins (antimicrobial peptides) and provide immunostimulation.26e29 Gram-positive obligate or facultative anaerobes are dominant in the gastrointestinal microbiota of man and terrestrial farm animals.30 Most probionts belong to dominant or sub-dominant genera among these microbiota, e.g., Bifidobacterium, Lactobacillus, Streptococcus.30 Gram-negative facultative anaerobes prevail in the digestive tract of fish and shellfish, though symbiotic anaerobes may be dominant in the posterior intestine of some herbivorous tropical fish.31 Vibrio and Pseudomonas are the most common genera in crustaceans,32 marine fish and bivalves.33,34 Aeromonas, Plesiomonas and Enterobacteriaceae are dominant in freshwater fish.33 Bacillus spp. hold added interest in probiotics as they can be kept in the spore form and therefore stored indefinitely on the shelf.35 The list of microorganism authorized as probiotics in feeding stuffs under Council Directive 70/524/EEC are given in Table 1. In addition, other probiotics are commercialized on the market that has been notified, but that do not appear in the last authorized list of feed additives published by the Commission.

5.

Mechanisms of action

Different modes of action or properties are desire on the potential probiotic like antagonism to pathogens36,37 ability of cells to produce metabolites (like vitamins) and enzymes,38 colonization or adhesion properties39 enhance the immune system.40

5.1.

Competitive exclusion of pathogenic bacteria

Competitive exclusion is a phenomenon whereby an established 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

Table 1 e List of microorganism authorized as probiotics in feeding stuffs under Council Directive 70/524/EEC. S. no. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.

Probiotic organism Bacillus cereus var. toyoi Bacillus licheniformis Bacillus subtilis Enterococcus faecium Lactobacillus casei Lactobacillus farciminis Lactobacillus plantarum Lactobacillus rhamnosus Pediococcus acidilactici Saccharomyces cerevisiae Streptococcus infantarius

competing bacterial challenge for the same location on the intestine. The aim of probiotic products designed under competitive exclusion is to obtain: stable, agreeable and controlled microbiota in cultures based on the following; competition for attachment sites on the mucosa, competition for nutrients and production of inhibitory substances by the microflora which prevents replication and/destroys the challenging bacteria and hence reduce colonization.12 Different strategies are displayed in the adhesion of microorganism to those attachment sites as passive forces, electrostatic interactions, hydrophobic, steric forces, lipoteichoic acids, adhesions and specific structures of adhesion.41Adhesion and colonization of the mucosal surfaces are possible protective mechanisms against pathogens through competition for binding sites and nutrients.42

5.2.

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natural or nonspecific defense system formed by a series of cellular and humoral components, and 2) the adaptive, acquired or specific immune system characterized by the humoral immune response through the production of antibodies and by the cellular immune response which is mediated by Tlymphocytes, capable of reacting specifically with antigens. The normal microbiota in the GI ecosystem influences the innate immune system, which is of vital importance for the disease resistance of fish and is divided into physical barriers, humoral and cellular components. Innate humoral parameters include antimicrobial peptides, lysozyme, complement components, transferring, pentraxins, lectins, antiproteases and natural antibodies, whereas nonspecific cytotoxic cells and phagocytes constitute innate cellular immune effectors. Cytokines are an integral component of the adaptive and innate immune response, particularly IL-1b, interferon, tumor necrosis factor-a, transforming growth factor-b and several cehmokines regulate innate immunity.44 The nonspecific immune system can be stimulated by probiotics. It has been demonstrated that oral administration of Clostridium butyricum bacteria to rainbow trout enhanced the resistance of fish to vibriosis, by increasing the phagocytic activity of leucocytes. Rengpipat et al, 20007 mentioned that the use of Bacillus sp. (strain S11) provided disease protection by activating both cellular and humoral immune defenses in tiger shrimp (Penaeus monodon). Balcazar, 200345 demonstrated that the administration of a mixture of bacterial strains (Bacillus and Vibrio sp.) positively influenced the growth and survival of juveniles of white shrimp and presented a protective effect against the immune system, by increasing phagocytosis and antibacterial activity.

Production of inhibitory compounds 5.4.

Bacterial antagonism is a common phenomenon in nature; therefore, microbial interactions play a major role in the equilibrium between competing beneficial and potentially pathogenic microorganisms.43 Antagonistic compounds are defined as chemical substances produced by microorganisms (in this case bacteria) that are toxic (bactericidal) or inhibitory (bacteriostatic) toward other microorganisms. The presence of bacteria producing antibacterial compounds in the intestine of the host, on its surface, or in its culture water is thought to prevent proliferation of pathogenic bacteria and even eliminate these. The structure of the antibacterial compound is often not elucidated and their mode of action has not been reported. Furthermore none of these reports demonstrate that the antibacterial compound is produced in vivo. This will be of significant importance, if production of these compounds and its mode of action are understood. If the production of antibacterial compound is the only mode of action, it is possible that the pathogen eventually will develop resistance toward the compound. This will result in an ineffective treatment. The risk of the pathogen to develop resistance against the active compound has to be evaluated, to assure a stable effect of the probiotic bacterium.

5.3. Enhancement of the immune response against pathogenic microorganisms The immune systems of fish and higher vertebrates are similar and both have two integral components: 1) the innate,

Antiviral effects

Some bacteria used as candidate probiotics have antiviral effects. Although the exact mechanism by which these bacteria exerts its antiviral effects is not known, laboratory tests indicates that the inactivation of viruses can occur by chemical and biological substances, such as extracts from marine algae and extracellular agents of bacteria. It has been reported that strains of Pseudomonas sp., Vibrio sp., Aeromonas sp., and groups of coryneforms isolated from salmonid hatcheries, showed antiviral activity against infectious hematopoietic necrosis virus (IHNV) with more than 50% plaque reduction.46 Girones et al, 198947 reported that a marine bacterium, tentatively classified in the genus Moraxella, showed antiviral activity against poliovirus. Direkbusarakim et al, 199848 isolated two strains of Vibrio spp. from a black tiger shrimp hatchery. These isolates displayed antiviral activities against IHNV and Oncorhynchus masou virus (OMV), with percentages of plaque reduction between 62 and 99%, respectively.

6.

Safety regulation

The safety profile of a potential probiotic strain is of critical importance in the selection process. This testing should include the determination of strain resistance to a wide variety of common classes of antibiotics such as tetracyclines, quinolones and macrolides and subsequent confirmation of

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non-transmission of drug resistance genes or virulence plasmids.49 Evaluation should also take the end-product formulation into consideration because this can induce adverse effects in some subjects or negate the positive effects altogether. A better understanding of the potential mechanisms whereby probiotic organisms might cause adverse effects will help to develop effective assays that predict which strains might not be suitable for use in probiotic products. Furthermore, modern molecular techniques should be applied to ensure that the species of probiotics used in aquaculture are correctly identified, for quality assurance as well as safety.

7.

Discussion

The application of probiotics in aquaculture shows promise, but needs considerable efforts of research. However, a number of probiotic products have been thoroughly researched, and evidenced their efficacy a possible use on aquaculture. Beneficial bacterial preparations that are species-specific probiotics have become more widely available to the aquaculture community. These preparations show specific beneficial effect as disease prevention and offer a natural element to obtain a stable healthy gut environment and immune system. The establishing of strong disease prevention program, including probiotic and good management practice can be beneficial to raise aquatic organism production.

8.

Conclusion

The application of probiotics in aquaculture shows promise, but needs considerable efforts of research. It is essential to understand the mechanisms of action in order to define selection criteria for potential probiotics. Therefore, more information on the host/microbe interactions in vivo, and development of monitoring tools (e.g. molecular biology) are still needed for better understanding of the composition and functions of the indigenous microbiota, as well as of microbial cultures of ‘‘probiotics’’. The use of probiotics is an important management tool, but its efficiency depends on understanding the nature of competition between species or strains.

Conflicts of interest All authors have none to declare.

Acknowledgments Authors are grateful to Rajiv Gandhi National Fellowship (F117.1/2011-12/RGNF-SC-TAM-1686/(SA-III Website)) University Grant Commission, Government of India, New Delhi for the financial support and sincere thanks and gratitude to Prof. Dr. T. Balasubramanian, Dean and Director, CAS in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai for the necessary facilities provided.

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