International Research Journal of Microbiology (IRJM) (ISSN: 2141-5463) Vol. 2(12) pp.

471-478, December, 2011 Special Issue

Available online http://www.interesjournals.org/IRJM
Copyright © 2011 International Research Journals

Review

The use of probiotic in aquaculture: an overview

Maurilio Lara-Flores
Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México. Universidad Autónoma de Campeche
Av. Agustín Melgar y Juan de la Barrera S/N. Col. Buenavista. C.P. 24039. San Francisco de Campeche, Campeche,
México.
E-mail: [email protected], [email protected]; Tel: +52 (981) 8119800 Ext. 62311.
Accepted 05 December, 2011

In last decade, the total world fishery production decreased slightly and the human consumption for
aquatic product increased. The reduction in capture fisheries was partly compensated for the fast
growth of aquaculture industry. The need for enhanced disease resistance, feed efficiency, and growth
performance of cultured organisms is substantial for various sectors of this industry. If growth
performance and feed efficiency are increased in commercial aquaculture, the costs productions are
likely to be reduced. Also if more aquatic organisms are able to resist diseases and survive the
subsequent cost of medication and overall production costs would be reduced. Hormones, antibiotics,
ionopheres and some salts compounds have been used at some extent to prevent disease and as
growth promoters; however, their inadequate application can produce adverse disorders, such as
hormone imbalance, poisoning and predisposition to disease development. In the search of new
options, several studies have been carried out to test new compounds, from which the aquaculture
industry has developed the concept of “functional additives”. Among these additives, the additions of
microorganisms to diets, named probiotics, has shown to improve the energy expenditure derived from
other sources such as carbohydrates and increase the incorporations of protein for growth; increase
the immunity and disease resistance of host organism. The use of probiotics in aquaculture just begum,
since that gastrointestinal microbiota of aquatic organisms has been poorly characterized; and their
effects not be study extensive. This review summarizes and evaluates current knowledge of use and the
action of probiotic in fish culture; and the potential for further application in aquaculture production.

Keywords: probiotic, bacteria, growth promoters, disease control, aquaculture

INTRODUCTION

Aquaculture is a fast-growing and rapidly expanding disease control measure in aquaculture. During the last
multibillion dollar industry. Marine capture fisheries and decades, antibiotics used as traditional strategy for fish
aquaculture supplied the world with about 104 million diseases management but also for the improvement of
tons of fish in 2004 (FAO, 2007). Of this total, marine growth and efficiency of feed conversion. However, the
aquaculture accounted for about 18%, where shrimp from development and spread of antimicrobial resistant
aquaculture continues to be the most important pathogens were well documented (Kim et al., 2004;
commodity traded in terms of value (2.4 million tons). Cabello, 2006; Sørum, 2006). There is a risk associated
Worldwide, the aquaculture sector has been expanding at with the transmission of resistant bacteria from
an average compounded rate of 9.2% per year since aquaculture environments to humans, and risk
1970, compared with only 1.4% for capture fisheries and associated with the introduction in the human
2.8% for terrestrial-farmed meat production systems. environment of nonpathogenic bacteria, containing
With the increasing intensification and antimicrobial resistance genes, and the subsequent
commercialization of aquaculture production, disease is a transfer of such genes to human pathogens (FAO, 2005).
major problem in the fish farming industry (Bondad- On other hand antibiotics inhibit or kill beneficial
Reantaso et al., 2005). Although vaccines are being microbiota in the gastrointestinal ecosystem it also made
developed and marketed, cannot be used as a universal antibiotic residue accumulated in fish products to be
472 Int. Res. J. Microbiol.

harmful for human consumption (WHO, 2006). noted by Tannock (1997), and he proposed the following
Considering these factors, as well as the fatal effect of definition “living microbial cells administered as dietary
residual antibiotics of aquaculture products on human supplement with the aim of improving health”.
health, the European Union and USA implemented bans The concept for aquatic probiotic is a relatively new.
on, or restricted the use of antibiotics (Kesarcodi-Watson When looking at probiotics for an aquatic usage it is
et al., 2008). The norms are stringent and there are many important to consider certain influencing factors that are
events of returning consignments to the exporting fundamentally different from terrestrial based probiotics.
countries for not maintaining the prescribed standards. Aquatic animals have much closer relationship with their
In connection with the ban of antibiotic growth external environment. There are the big differences
promoters new strategies in feeding and health between terrestrial and aquatic animals in the level of
management in fish aquaculture practice have received interaction between the intestinal microbiota and the
much attention (Balcázar et al., 2006). In addition, the surrounding environment. Potential pathogens are able to
global demand for safe food has prompted the search for maintain themselves in the external environment of the
natural alternative growth promoters to be used in aquatic animal (water) and proliferate independently of the host
feeds. There has been heightened research in animal (Hansen and Olafsen, 1999; Verschuere et al.,
developing new dietary supplementation strategies in 2000). These potential pathogens are taken up constantly
which various health and growth promoting compounds by the animal through the processes of osmoregulation
as probiotics, prebiotics, synbiotics, phytobiotics and and feeding. The bacterial community composition of the
other functional dietary supplements have been intestinal tract of aquatic animals is different from that
evaluated (Denev, 2008). found in terrestrial animals, which the probiotic concept
In this context, microbial intervention can play a vital was developed. Man and terrestrial livestock undergo
role in aquaculture production, and effective probiotic embryonic development within an amnion, whereas the
treatments may provide broad spectrum and greater larval forms of most fish and shellfish are released in the
nonspecific disease protection (Rengpipat et al., 2000; external environment at an early ontogenetic stage.
Panigrahi and Azad, 2007). The range of probiotic These larvae are highly exposed to gastrointestinal
microorganisms examined for use in aquaculture includes microbiota-associated disorders, because they start
both Gram-negative and Gram-positive bacteria, feeding even though the digestive tract is not yet fully
bacteriophages, yeasts, and unicellular algae (Irianto and developed (Timmermans, 1987), and though the immune
Austin, 2002). The selection for probiotic candidate system is still incomplete (Vadstein, 1997). Thus,
organisms was based on in vitro antagonism (Vershuere probiotic treatments are particularly desirable during the
et al., 2000), as well as on the results of adhesion, larval stages (Gatesoupe, 1999). A study with Atlantic
colonization, and growth in intestinal mucus (Irianto and halibut (Hippoglossus hippoglossus) showed the
Austin, 2002; Vine et al., 2004). transition from a prevailing Flavobacterium spp. intestinal
This review summarizes and evaluates current flora to an Aeromonas spp. and Vibrio spp. dominant
knowledge of the use and the action of the probiotic in flora occurred when first feeding commenced (Bergh et
aquaculture; and the potential for further application of al., 1994). This study highlighted the impact that the
this in production. external environment and feeding had on the microbial
status of fish. However, the same study also found that
larvae did maintain a specific intestinal flora different to
Definition of probiotic that of the external tank flora. This showed that, although
there were ever-present external environmental factors
The term probiotic means “for life,” originating from Greek influencing the microbial flora inside an aquatic animal,
words “pro” and “bios” (Gismondo et al., 1999). The they could still maintain a host specific flora at any given
concept of probiotic was originally used by Lilley and time. It was suggested that this ability did not apply to
Stillwell (1965) to mean a substance (s) that stimulates bivalve larvae (Jorquera et al., 2001). Their work
growth of other microorganisms (Chukeatirote, 2002). demonstrated that the transit time of bacteria in bivalve
Parker in 1974 modified the definition to “organisms and larvae was too short to allow the establishment of a
substances which contribute to intestinal balance”. Fuller bacterial population different from that of surrounding
(1992) revised the definitions as “ A live microbial feed water.
supplement which beneficially effects the host animal by Based on the intricate relationship an aquatic organism
improving its intestinal microbial balance”. This definition has with the external environment when compared with
has put forward the importance of live cells as the that of terrestrial animals, the definition of a probiotic for
essential component of a potential probiotic and its clears aquatic environments needs to be modified. Gatesoupe
the confusion created by the use of term “substance”. (1999) redefined probiotics for aquaculture as “Microbial
However, an effect in intestinal microbial balance has cells that are administered in such a way as to enter the
been defined and demonstrated only in few cases. This gastrointestinal tract and to be kept alive, with the aim of
 Lara-Flores 473

improving health”. The definition of Gatesoupe is focuses Eubacterium (Sakata, 1990). Lactic acid producing
on the oral delivery of the probiotic and its ability to bacteria, which are prevalent in the mammal or bird gut,
improve the health of the host as a result of its presence are generally sub-dominant in fishes and represented
in the digestive tract. Verschuere et al. (2000) suggested essentially by the genus Carnobacterium (Ringo and
the definition “a live microbial adjunct which has a Vadstein, 1998).
beneficial effect on the host by modifying the host Ideally, microbial probiotics should have a beneficial
associated or ambient microbial community, by ensuring effect and not cause any harm to the host. Therefore, all
improved use of the feed or enhancing its nutritional strains have to be non-pathogenic and non-toxic in order
value, by enhancing the host response towards disease, to avoid undesirable side-effects when administrated to
or by improving the quality of its ambient environment”. A aquatic animals.
part from the requirement of the probiotic to be a live Some research and products talk about the
culture, this definition is a lengthy way of describing a multifactorial action of the probiotics (Gomez et al., 2007;
probiotic as defined by Irianto and Austin (2002) thus “a Tuohy et al. 2003) on aquatic animals. However, the
probiotic is an entire or components of a microorganism multifactorial effect is not agreed with evidence or is
that is beneficial to health of the host”. Other definitions in overestimate. Sometimes, this type of publicity about of
aquaculture show that probiotic is a live microbial food those products really affects the perspective of real
supplements that are consumed with the aim of providing probiotic designed for aquaculture industry.
health benefit to the host by contributing to an improved Different modes of action or properties are desire on
microbial balance within the intestinal microbiota (Gram the potential probiotic like antagonism to pathogens
et al., 1999; Crittenden et al., 2005), are biologically (Ringo and Vadstein, 1998; Gram and Melchirosen,
active components or single or mixed cultures of 1996), ability of cells to produce metabolites (like
microorganism capable of improving the health of the vitamins) and enzymes (Ali, 2000), colonization or
host (Salminen et al., 1999; Ochoa-Solano and Olmos- adhesion properties (Olsson et al., 1992) enhance the
Soto, 2006), live microorganisms and/or disease immune systems (Perdigon et al., 1995) and other.
resistance (Tacon, 2002), live microorganisms
administered in adequate amounts that confer a health
effect on the host (Gomez et al., 2007). These definitions Competitive exclusion
reflect the use of microorganism or their products
(microbial cells element or cell free supernatant factors) Competitive exclusion as it applies to the gastrointestinal
to tanks and ponds in which animals live, as biological tract is a phenomenon whereby an established microflora
control or their capacity of modified the bacterial prevents or reduces the colonization of a competing
composition of aquatic animal´s intestine, water and bacterial challenge for the same location on the intestine.
sediment, or used with feed as health supplement and/or This microflora begins to form in the gut of aquatic
biological control. animals during the hatching process and shortly
thereafter form bacteria in the environment.
The aim of probiotic products designed under
Criteria of probiotic selection in aquaculture competitive exclusion is obtain stable, agree and
controlled microbiota on culture based on competition for
The initial, major, purpose of using probiotics is to attachment sites on the mucosa, competition for
maintain or reestablish a favorable relationship between nutrients, and production of inhibitory substance by the
friendly and pathogenic microorganisms that constitute microflora which prevents replication and/or destroys the
the flora of intestinal o skin mucus of aquatic animals. challenging bacteria and with this reduce its colonization
Since, successful probiotic is expected to have a few (Moriarty, 1998; Verschuere et al., 2000). Different
specific properties in order to certify beneficial effects (Ali, strategies are displayed in the adhesion of
2000). microorganism to those attachment sites as passive
Generally, probiotic strains have been isolated from forces, electrostatic interactions, hydrophobic, steric
indigenous and exogenous microbiota of aquatic animals. forces, lipoteichoic acids, adhesions and specific
Gram-negative facultative anaerobic bacteria such as structures of adhesion (Salyers and White, 2002).
Vibrio and Pseudomonas constitute the predominant The aquaculture industry display some probiotics
indigenous microbiota of a variety of species of marine products designed to adhesion on mucosal surface by a
animals (Onarheim, 1994). In contrast to saltwater collection of microorganisms based on the competitive
organisms, the indigenous microbiota of freshwater exclusion factors (Verschuere et al., 2000; Farzanfar,
animals tends to be dominated by member of the genera 2004). Those factors are important for adhesion to
Aeromonas, Plesiomonas, representatives of the family intestinal epithelial cells or in the activation of immune
Enterobacteriaceae, and obligate anaerobic bacteria of system, and help to the health of the organisms, intestinal
the genera Bacteroides, Fusubacterium, and homeostasis, and digestion (Aguirre-Guzman, 1992;
474 Int. Res. J. Microbiol.

Farzanfar, 2004). These types of probiotic are extensively biochemical activities along their development and based
study in fish since these products were initialed on environments (fresh, seawater) and original source.
development for vertebrate animals, and show interesting These characteristics affect the probiotic potential for
results. attachment sites (Vanbelle et al., 1990) an may create a
false impression of the ability of probiotics to inhibit in
vivo test. The probiotics screening preferably requires
Antagonisms different stategy of selection as antagonism, production
of beneficial compounds, attachment and growth on
Control of microbial communities with high diversity has various environments (Vine et al., 2004).
been regarded as difficult (Maeda et al., 1997). Such
types of microbial communities can disperse the effect
caused by the invasion or addition of certain extrinsic Immunity stimulation
pathogenic organisms. Bacterial antagonism is a
common phenomenon in nature; therefore, microbial The immune systems of fish and higher vertebrates are
interactions play a major role in the equilibrium between similar and both have two integral components: 1) the
competing beneficial and potentially pathogenic innate, natural or nonspecific defense system formed by
microorganisms (Balcazar et al., 2004). In addition, a series of cellular and humoral components, and 2) the
microorganisms can be sources of a variety of bioactive adaptive, acquired or specific immune system
natural products of basic research and commercial characterized by the humoral immune-response through
interest that have inhibitory effects on microbial growth the production of antibodies and by the cellular immune
(Das et al., 2006). response which is mediated by T-lymphocytes, capable
Antagonistic compounds are defined as chemical of reacting specifically with antigens. The normal
substances produced by microorganisms (in this case microbiota in the GI ecosystem influences the innate
bacteria) that are toxic (bactericidal) or inhibitory immune system, which is of vital importance for the
(bacteriostatic) towards other microorganisms. The disease resistance of fish and is divided into physical
presence of bacteria producing antibacterial compounds barriers, humoral and cellular components. Innate
in the intestine of the host, on its surface, or in its culture humoral parameters include antimicrobial peptides,
water is thought to prevent proliferation of pathogenic lysozyme, complement components, transferring,
bacteria and even eliminate these. The antibacterial pentraxins, lectins, antiproteases and natural antibodies,
compounds can be divided into compound with a direct or whereas nonspecific cytotoxic cells and phagocytes
indirect effect on the pathogen. Lactic acid bacteria often constitute innate cellular immune effectors. Cytokines are
produce bacteriocins, however, these are often only an integral component of the adaptive and innate immune
active against closely realted species (Klaenhammer, response, particularly IL-1β, interferon, tumor necrosis
1993) and most pathogens involved in aquaculture are factor-α, transforming growth factor-β and several
Gram-negative and bacteriocins from lactic acid bacteria cehmokines regulate innate immunity (Gomez and
may therefore not inhibit fish pathogenic bacteria. Balcazar, 2008).
Probiotic bacteria suggested as probiotic treatment in The non-specific immune system can be stimulated by
aquaculture can produce both proteinaceous and non- probiotics. It has been demonstrated that oral
proteinaceous substrates. The structure of the administration of Clostridium butyricum bacteria to
antibacterial compound is often not elucidated and their rainbow trout enhanced the resistance of fish to vibriosis,
mode of action has not been reported. Furthermore none by increasing the phagocytic activity of leucocytes (Sakai
of these reports demonstrate that the antibacterial et al. 1995). Rengpipat et al., (2000) mentioned that the
compound is produced in vivo. This will be of significant use of Bacillus sp. (strain S11) provided disease
importance if production of these compounds is the mode protection by activating both cellular and humoral
of action. If the production of antibacterial compound is immune defenses in tiger shrimp (Penaeus monodon).
the only mode of action, it is possible that the pathogen Balcazar (2003) demonstrated that the administration of a
eventually will develop resistance towards the compound. mixture of bacterial strains (Bacillus and Vibrio sp)
This will result in an ineffective treatment. The risk of the positively influenced the growth and survival of juveniles
pathogen to develop resistance against the active of white shrimp and presented a protective effect against
compound has to be evaluated, to assure a stable effect the immune system, by increasing phagocytosis and
of the probiotic bacterium. antibacterial activity. In addition, Nikoskelainen et al.
In the other hand, the origin of probiotic strain is an (2003) showed that administration of a lactic acid
important element in the antagonisms test. The bacterium Lactobacillus rhamnosus at a level of 105 cfu/g
microorganism present different physiologies or feed, stimulated the respiratory burst in rainbowtrout.
 Lara-Flores 475

Antiviral effects to mucus, gastrointestinal tract, epithelial cell and other

tissues is a common characteristic in the probiotic
Some bacteria used as candidate probiotics have selection because it is assicuated with bacteria
antiviral effects. Although the exact mechanism by which colonization (Verschuere et al., 2000; Farzanfar, 2004;
these bacteria do this is not know, laboratory test indicate Crittenden et al., 2005).
that the inactivation of viruses can occur by chemical and The principal objective of adhesion is obtain a
biological substances, such as extracts from marine significant level of bacteria in the host and prevents them
algae and extracellular agents of bacteria. It has been from being flushed out by the movement of food through
reported that strains of Pseudomonas sp., Vibrio sp., the digestive tract. By attaching to the intestinal mucosa,
Aeromonas sp., and groups of coryneforms isolated from probiotics can extend their time within the gut thereby
salmonid hatcheries, showed antiviral activity against influence the gastrointestinal microflora of their host
infectious hematopoietic necrosis virus (IHNV) with more (Andlid et al., 1998; Ouwehan et al., 2000; Rengpipat et
than 50% plaque reduction (Kamei et al., 1988). Girones al., 2003; Alavandi et al, 2004).
et al. (1989) reported that a marine bacterium, tentatively The attachment ability of some bacteria have been
classified in the genus Moraxella, showed antiviral tested in vitro and in vivo and their results suggest that
capacity, with high specificity for poliovirus. the pathogen was displaced by the potential probiotic,
Direkbusarakim et al. (1998) isolated two strains of Vibrio based on the ability of probiotic to attach to the mucus,
spp. from a black tiger shrimp hatchery. These isolates where growth of the pathogen in the digestive tract might
displayed antiviral activities against IHNV and be suppressed by the candidate probiotic presence
Oncorhynchus masou virus (OMV), with percentages of (Aguirre-Guzman, 1992; Verschuere et al., 2000;
plaque reduction between 62 and 99%, respectively. Farzanfar, 2004; Vine et al., 2004). This characteristic is
associated with the competition for essential nutrient,
space, etc. (Verschuere et al., 2000). Different strains of
Adhesion acid lactic bacteria, like Enterococcus faecium and
Lactobacillus sp.; and other groups of bacteria Gram-
Probiotics make up part of the resident microflora and positive and Gram negative as Bacillus sp., Vibrio sp.,
contribute to the health or well-being of their host have been tested and posteiori used as probiotic for the
(Gatesoupe, 1999). The ability of some strain of adhesion ability of adhesion (Irianto and Austin, 2002, Rengpipat et
to mucus, gastrointestinal tract, epithelial cell and other al., 2003; Ajitha et al,. 2004; Vine et al. 2004).
tissues is a common characteristic in the probiotic
selection because it is associated with bacteria
colonization (Verschuere et al., 2000; Farzanfar, 2004; Digestive process
Crittenden et al., 2005).
Colonization of the gastrointestinal trace of animals by Many studies on probiotics in aquaculture have used in
probiotics is possible only after birth, and before the vitro models of specific bacteria as antagonists of
definitive installation of a very competitive indigenous pathogens (Vine et al., 2004; 2006), measured the
microbiota. After this installation, only the addition of high survival of probiotics in the fish gut (Andlid et al., 1998) or
doses of probiotic provokes its artificial and temporary evaluated the effect of probiotic on health management,
dominance. In mature animals, the population of probiotic disease resistance and immune response of fish (Li and
organisms in the gastrointestinal tract shows a sharp Gatlin III, 2004; Shelby et al., 2006). But other important
decrease within days after the intake had stopped (Fuller, effect of probiotic that it is not extensively study, but
1992). According to Conway (1996), a microorganism is demonstrated, an import effect is the feed efficiency and
able to colonize the gastrointestinal tract when it can the growth promotion of aquatic animals by probiotic
persist there for a long time, by possessing a supplements (Gatesoupe, 2002; Lara-Flores et al., 2003).
multiplication rate that is higher than its expulsion rate. The probiotic after transit through the stomach,
The process of colonization is characterized by attached in the intestine and use a large number of
attraction of bacteria to the mucosal surface, followed by carbohydrates for their growth and produce relevant
association within the mucous gel or attachment to digestive enzymes (amylase, protease and lipase) that
epithelial cells. Adhesion and colonization of the mucosal increase the digestibility of organic matter and protein,
surfaces are possible protective mechanisms against produce a higher growth, prevent the intestinal disorders
pathogens through competition for binding sites and and produce or/and stimulate a predigestion of secondary
nutrients (Westerdahl et al., 1991), or immune modulation compounds present in plant protein sources (Lara-Flores
(Salminen et al., 1999). et al., 2003; El-Haroun et al., 2006).
Probiotics make up part of the resident microflora and In fish the use of probiotics demonstrated beneficial
contribute to the health or well-being of their host effects on the growth performance, feed efficiency and
(Gatesoupe, 1999). The ability of some strain of adhesion digestibility of organic matter and protein, when used acid
476 Int. Res. J. Microbiol.

lactic bacteria and yeast (Vazquez-Juarez et al., 1993; understand before massive application on aquaculture.
Noh et al., 1994; Bogout et al., 1998; Ringo and However, a number of probiotic products have been
Gatesoupe, 1998; De Schrijver and Ollevier, 2000; Lara- thoroughly researched, and evidenced their efficacy a
Flores et al. 2003). In some case this effect attributed to possible use on aquaculture. Beneficial bacterial
the capacity of the probiotic to stimulate and/or produce preparations that are species-specific probiotics have
some enzymes in the intestinal tract. For example, in fish become more widely available to the aquaculture
it has reported that Bacteroides and Clostridium sp. have community. These preparation show specific benefic
contributed to the host´s nutrition, especially by supplying effect as disease prevention and offer a natural element
fatty acids and vitamins (Sakata, 1990). Some to obtain a stab le healthy gut environment and immune
microorganisms such as Agrobacterium sp., system. The establishing of strong disease prevention
Pseudomonas sp., Brevibacterium sp., Microbacterium program, including probiotic and good management
sp., and Staphylococcus sp. may contribute to nutritional practice can be beneficial to raise aquatic organism
processes in Arctic charr (Salvelinus alpines L.) (Ringo et production.
al, 1995). Lara et al. (2010) observed a high activity of
alkaline phosphatase in Nile tilapia (Oreochromis
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