Elsevier

Aquaculture

Volume 302, Issues 1–2, 1 April 2010, Pages 1-18
Aquaculture

Review
The current status and future focus of probiotic and prebiotic applications for salmonids

https://doi.org/10.1016/j.aquaculture.2010.02.007Get rights and content

Abstract

Salmonids are an important contributor to fish production in many countries. Concerted research efforts have concentrated on optimising production with eco-friendly alternatives to the therapeutic use of antimicrobials. Probiotics and prebiotics offer potential alternatives by providing benefits to the host primarily via the direct or indirect modulation of the gut microbiota. Suggested modes of action resulting from increased favourable bacteria (e.g. lactic acid bacteria and certain Bacillus spp.) in the gastrointestinal (GI) tract include the production of inhibitory compounds, competition with potential pathogens, inhibition of virulence gene expression, enhancing the immune response, improved gastric morphology and aiding digestive function. The application of probiotics and prebiotics may therefore result in elevated health status, improved disease resistance, growth performance, body composition, reduced malformations and improved gut morphology and microbial balance.

Current research demonstrates successful proof of these concepts and a foundation for applications in salmonid aquaculture. However, application strategies applied in current studies are varied and often impractical at industrial level farming; thus, it is difficult to plan an effective feeding strategy for commercial level applications. Future studies should focus on providing practical industrial scale applications. Additionally, from a scientific perspective we must have a better understanding of the mucosal–bacterial interactions which mediate the host benefits in order to achieve optimal utilisation.

Introduction

Although there is now global recognition that aquaculture production is expanding to a wide diversity of cultured finfish, salmonids remain an important contributor to fish production in many countries. Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss W.) are reared principally in Norway, Scotland and Chile with some output arising from Canada, the USA, regions of Europe and to a lesser extent Australia and New Zealand. Total global production of salmonids was reported to exceed 2.2 million mt in 2007 (FAO, 2009). These species attract high market prices and are a stable source of high quality fish due to consumer acceptance for quality seafood. Salmon in particular are noteworthy for their characteristic pink-reddish flesh pigmentation (Davies, 2008) and versatility with respect to processing into a wide range of food products. Rainbow trout is also a popular salmonid fish species and has received great attention in terms of importance to aquaculture and remain a core of inland fish production in many countries throughout the world. It should also be recognised that native species of brown trout (Salmo trutta) are important especially in terms of their contribution to recreational fisheries and angling. Additionally, developments in rearing techniques for Arctic charr (Salvelinus alpinus) have increased interest in commercial farming and consequently global production has risen to over 2000 mt in 2007 (Jobling et al., 1993, FAO, 2009). Collectively, there has been an abundance of scientific literature underpinning the genetics, nutrition, health and disease issues concerning the development of the salmonid aquaculture industry.

Given the importance of nutrition in maintaining the health of fish, with respect to nutritional involvement on immuno-competence and disease resistance, as well as its role in stress mediation, there is a growing trend towards exploring dietary components of a non-nutritional nature to provide various functional attributes. This has been compounded by the constraints of employing antibiotics in the aquaculture industry, as reflected by the EU moratorium on the banning of antibiotic growth promoters in animal feeds, including fish (Regulation, EC No, 1831).

There have been numerous investigations on salmon and trout to evaluate the feasibility of supplementing diets with a range of potentially probiotic bacteria. Several general reviews have been published over the past decade summarising the latest available literature (Ringø and Gatesoupe, 1998, Gatesoupe, 1999, Ringø and Birkbeck, 1999, Vershuere et al., 2000, Irianto and Austin, 2002a, Ringø, 2004, Burr et al., 2005, Balcázar et al., 2006a, Gram and Ringø, 2005, Ringø et al., 2005, Gatesoupe, 2007, Kesarcodi-Watson et al., 2008, Wang et al., 2008a). Furthermore, specific reviews have focused on larvae (Gomez-Gil et al., 2000, Vine et al., 2006, Tinh et al., 2008), shrimp (Farzanfar, 2006, Ninawe and Selvin, 2009), shellfish (Balcázar et al., 2006b) along with reviews specific to applications for Indian (Panigrahi and Azad, 2007) and Chinese aquaculture (Qi et al., 2009). However, to the authors' knowledge, no reviews have been put forward to summarise the effects of probiotics on salmonids. Additionally, with the growing interest and assessment of prebiotic applications for fish, it is pertinent to review the present findings with regards to salmonid fish.

The aim of this review is to evaluate the literature currently available regarding the use of probiotics and prebiotics (collectively referred to as “biotics” hereafter) on salmonids. Specific emphasis is placed on highlighting application strategies on a practical basis and potential future research. In order to discuss these issues we must first examine the complex microbe–host interactions within the gut, which ultimately influence the health and development of the host.

Section snippets

Endogenous microbiota, mucosal tolerance and development

The immune system of teleost fish appears to be an efficient means by which the host protects itself upon pathogenic challenge. But not all microbes represent a pathogenic threat; resident commensal microbes help maintain efficient functioning of the gut by supporting gut mucosal barrier function: mounting efficient immune responses to pathogens that break through barrier defences or maintaining tolerance (i.e. immune non-responsiveness) to luminal contents which allow for nutrient absorption.

Probiotics

The word probiotic is constructed from the Latin word pro (for) and the Greek word bios (life) (Zivkovic, 1999). The definition of a probiotic differs greatly depending on the source, but the first generally accepted definition was proposed by Fuller (1989) as “…a live microbial feed supplement which beneficially affects the host animal by improving its microbial balance”. Given the nature of fish farming and the fact that water harbours microbial communities it is accepted that we must have a

Prebiotics

The use of probiotics in many cases, as discussed previously, may be difficult in commercial aquaculture because of the low viability of the bacteria after pelleting and during storage, leaching from the feed particle in rearing water, as well as problems related with feed handling and preparation. As an alternative (or also considered for use in tandem: synbiotics), prebiotics have been assessed in an attempt to overcome issues associated with probiotic applications. From an endothermic point

Synbiotics

Synbiotics, the combined application of probiotics and prebiotics, is based on the principle of providing a probiont with a competitive advantage (a fermentable energy source) over competing endogenous populations; Thus, effectively improving the survival and implantation of the live microbial dietary supplement in the gastrointestinal tract of the host (Gibson and Roberfroid, 1995). To the authors knowledge only one synbiotic study has been conducted in salmonids (Rodriguez-Estrada et al., 2009

Concluding remarks and future perspectives

Current research provides a foundation but applications within these studies are often impractical at industrial level farming that it is difficult to plan feeding strategies for commercial level applications. Future efforts must focus on implementing more practical applications as well as scientific studies designed to understand the mechanisms that underpin and mediate the observed host benefits. In this context, growth performance parameters and body composition analysis should be

Acknowledgements

The authors, as well as their respective institutions, would like to dedicate this article to their dear departed colleague and friend, Bruno Rochet (who died on 5 November 2009 at the age of 55 years). Bruno was the business development director for Lallemand Animal Nutrition, having joined Lallemand in 1998, after numerous years of working on the use of probiotics in Animal Nutrition. He was the founder and first president of the European Probiotic Association established in 1999. As one of

References (188)

  • F.-J. Gatesoupe

    Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development

    Aquacult.

    (2007)
  • G.R. Gibson et al.

    Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics

    J. Nutr.

    (1995)
  • A. Gildberg et al.

    Effects of supplementing the feed to Atlantic cod (Gadus morhua) fry with lactic acid bacteria and immuno-stimulating peptides during a challenge trial with Vibrio anguillarum

    Aquacult.

    (1998)
  • A. Gildberg et al.

    Growth and survival of Atlantic salmon (Salmo salar) fry given diets supplemented with fish protein hydrolysate and lactic acid bacteria during a challenge trial with Aeromonas salmonicida

    Aquacult.

    (1995)
  • B. Gomez-Gil et al.

    The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms

    Aquacult.

    (2000)
  • L. Gram et al.

    In vitro antagonism of the probiont Pseudomonas fluorescens strain AH2 against Aeromonas salmonicida does not confer protection of salmon against furunculosis

    Aquacult.

    (2001)
  • L. Gram et al.

    Prospects of fish probiotics

  • B. Grisdale-Helland et al.

    The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar)

    Aquacult.

    (2008)
  • H.A. Hong et al.

    The use of bacterial spore formers as probiotics

    FEMS Microbiol. Rev.

    (2005)
  • B. Hyronimus et al.

    Acid and bile tolerance of spore-forming lactic acid bacteria

    Int. J. Food Mirobiol.

    (2000)
  • A. Kesarcodi-Watson et al.

    Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes

    Aquacult.

    (2008)
  • D.-H. Kim et al.

    Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics

    Fish Shellfish Immunol.

    (2006)
  • D.-H. Kim et al.

    Cytokine expression in leucocytes and gut cells of rainbow trout, Oncorhynchus mykiss Walbaum, induced by probiotics

    Vet. Immunol. Immunopathol.

    (2006)
  • G. Kurath et al.

    Protective immunity and lack of histopathological damage two years after DNA vaccination against infectious hematopoietic necrosis virus in trout

    Vaccine

    (2006)
  • M. Lara-Flores et al.

    Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus)

    Aquacult.

    (2003)
  • P. Li et al.

    Evaluation of the prebiotic GroBiotic®-A and brewers yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysops × M. saxatilis) challenged in situ with Mycobacterium marinum

    Aquacult.

    (2005)
  • P. Li et al.

    Dietary supplementations of short-chain fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of pacific white shrimp Litopenaeus vannamei, cultured in a recirculating system

    J. Nutr.

    (2007)
  • J. Li et al.

    Dietary probiotic Bacillus OJ and isomaltooligosaccharides influence the intestine microbial populations, immune responses and resistance to white spot syndrome virus in shrimp (Litopenaeus vannamei)

    Aquacult.

    (2009)
  • N. Lorenzen et al.

    Immunity to rhabdoviruses in rainbow trout: the antibody response

    Fish Shellfish Immunol.

    (1999)
  • M.J. Mauel et al.

    Piscirickettsiosis and piscirickettsiosis-like infections in fish: a review

    Vet. Microbiol.

    (2002)
  • M.R. Adams

    Safety of industrial lactic acid bacteria

    J. Biotechnol.

    (1999)
  • T. Andlid et al.

    Yeast colonizing the intestine of rainbow trout (Salmo gairdneri) and turbot (Scophtalmus maximus)

    Microb. Ecol.

    (1995)
  • S. Arijo et al.

    Subcellular components of Vibrio harveyi and probiotics induce immune responses in rainbow trout, Oncorhynchus mykiss (Walbaum), against V. harveyi

    J. Fish Dis.

    (2008)
  • J. Aubin et al.

    Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum)

    Aquacult. Res.

    (2005)
  • J. Aubin et al.

    Étude de l'amélioration de la rentabilité et de la sécurité sanitaire des filières truite arc-en-ciel et bar par l'utilisation de probiotiques par voie alimentaire

  • B. Austin et al.

    A probiotic strain of Vibrio alginolyticus effective in reducing diseases caused by Aeromonas salmonicida, Vibrio anguillarum and Vibrio ordalii

    J. Fish Dis.

    (1995)
  • T. Bagheri et al.

    Growth, survival and gut microbial load of rainbow trout (Onchorhynchus mykiss) fry given diet supplemented with probiotic during the two months of first feeding

    Turk. J. Fish. Aquat. Sci.

    (2008)
  • A.M. Bakke-McKellep et al.

    Effects of dietary soybean meal, inulin and oxytetracycline on gastrointestinal histological characteristics, distal intestine cell proliferation and intestinal microbiota in Atlantic salmon (Salmo salar L.)

    Brit. J. Nutr.

    (2007)
  • J.L. Balcázar et al.

    Health and nutritional properties of probiotics in fish and shellfish

    Microb. Ecol. Health Dis.

    (2006)
  • J.L. Balcázar et al.

    Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta)

    Brit. J. Nutr.

    (2007)
  • J.L. Balcázar et al.

    Enhancement of the immune response and protection induced by probiotic lactic acid bacteria against furunculosis in rainbow trout (Oncorhynchus mykiss) FEMS

    Immunol. Med. Microbiol.

    (2007)
  • J.L. Balcázar et al.

    Effect of Lactococcus lactis CLFP 100 and Leuconostoc mesenteroides CLFP 196 on Aeromonas salmonicida infection in brown trout (Salmo trutta)

    J. Mol. Microbiol. Biotechnol.

    (2009)
  • E. Benediktsdottir et al.

    Characterization of Vibrio viscosus and Vibrio wodanis isolated at different geographical locations: a proposal for reclassification of Vibrio viscosus as Moritella viscosa comb

    Nov. Int. J. Syst. Evol. Microbiol.

    (2000)
  • I. Bogut et al.

    Influence of probiotic (Streptococcus faecium M74) on growth and content of intestinal microflora in carp (Cyprinus carpio) Czech

    J. Animal Sci.

    (1998)
  • I. Bogut et al.

    Effects of Enterococcus faecium on the growth rate and intestinal microflora in sheat fish (Silurus glanis)

    Vet. Med.

    (2000)
  • D.W. Bruno et al.

    Histopathology, bacteriology and experimental transmission of a cold water vibriosis in Atlantic salmon Salmo salar

    Dis. Aquat. Org.

    (1986)
  • J. Brunt et al.

    Use of a probiotic to control lactococcosis and streptococcosis in rainbow trout, Oncorhynchus mykiss (Walbaum)

    J. Fish Dis.

    (2005)
  • J. Brunt et al.

    The development of probiotics for the control of multiple bacterial diseases of rainbow trout, Oncorhynchus mykiss (Walbaum)

    J. Fish Dis.

    (2007)
  • G. Burr et al.

    Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture

    J. World Aquac. Soc.

    (2005)
  • G. Burr et al.

    A preliminary in vitro assessment of GroBiotic®-A, brewer's yeast and fructooligosaccharide as prebiotics for the red drum Sciaenops ocellatus

    J. Environ. Sci. Health

    (2008)
  • Cited by (0)

    View full text