Abstract
To better understand salmon GI tract microbial community dynamics in relation to diet, a feeding trial was performed utilising diets with different proportions of fish meal, protein, lipid and energy levels. Salmon gut dysfunction has been associated with the occurrence of casts, or an empty hind gut. A categorical scoring system describing expressed digesta consistency was evaluated in relation to GI tract community structure. Faster growing fish generally had lower faecal scores while the diet cohorts showed minor differences in faecal score though the overall lowest scores were observed with a low protein, low energy diet. The GI tract bacterial communities were highly dynamic over time with the low protein, low energy diet associated with the most divergent community structure. This included transiently increased abundance of anaerobic (Bacteroidia and Clostridia) during January and February, and facultatively anaerobic (lactic acid bacteria) taxa from February onwards. The digesta had enriched populations of these groups in relation to faecal cast samples. The majority of samples (60–86 %) across all diet cohorts were eventually dominated by the genus Aliivibrio. The results suggest that an interaction between time of sampling and diet is most strongly related to community structure. Digesta categorization revealed microbes involved with metabolism of diet components change progressively over time and could be a useful system to assess feeding responses.
Similar content being viewed by others
Abbreviations
- GI:
-
Gastrointestinal
- DE:
-
Digestible energy
- SGS:
-
Summer Gut Syndrome
References
ABARES (2013) Australian Fisheries and Aquaculture Statistics 2012 (ABARES): pp. 119. Australian Bureau of Agricultural and Resource Economics, Canberra, Australia
Green TJ, Smullen R, Barnes AC (2013) Dietary soybean protein concentrate-induced intestinal disorder in marine farmed Atlantic salmon, Salmo salar is associated with alterations in gut microbiota. Vet Microbiol 166:286–292
Tacon AG, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158
Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776
Barton BA, Schreck CB, Fowler LG (1988) Fasting and diet content affect stress-induced changes in plasma glucose and cortisol in juvenile chinook salmon. Prog Fish Cult 50:16–22
Gomez D, Sunyer JO, Salinas I (2013) The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immun 35:1729–1739
Sullam KE, Essinger SD, Lozupone CA, O’Connor MP, Rosen GL, Knight R, Kilham SS, Russell JA (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21:3363–3378
De Cruz P, Prideaux L, Wagner J, Ng SC, McSweeney C, Kirkwood C, Morrison M, Kamm MA (2012) Characterization of the gastrointestinal microbiota in health and inflammatory bowel disease. Inflamm Bowel Dis 18:372–390
Kostic AD, Howitt MR, Garrett WS (2013) Exploring host-microbiota interactions in animal models and humans. Genes Dev 27:701–718
Hermes G, Zoetendal E, Smidt H (2014) Molecular ecological tools to decipher the role of our microbial mass in obesity. Benef Microbes 5:1–21
Joyce SA, Gahan CG (2014) The gut microbiota and the metabolic health of the host. Curr Opin Gastroen 30:120–127
Clements KD, Angert ER, Montgomery WL, Choat JH (2014) Intestinal microbiota in fishes: what’s known and what’s not. Mol Ecol 23:1891–1898
Ray A, Ghosh K, Ringø E (2012) Enzyme‐producing bacteria isolated from fish gut: a review. Aquacult Nutr 18:465–492
Muñoz-Atienza E, Gómez-Sala B, Araújo C, Campanero C, Del Campo R, Hernández PE, Herranz C, Cintas LM (2013) Antimicrobial activity, antibiotic susceptibility and virulence factors of lactic acid bacteria of aquatic origin intended for use as probiotics in aquaculture. BMC Microbiol 13:15
Geraylou Z, Souffreau C, Rurangwa E, De Meester L, Courtin CM, Delcour JA, Buyse J, Ollevier F (2013) Effects of dietary arabinoxylan-oligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baerii). Fish Shellfish Immun 35:766–775
Pérez T, Balcázar J, Ruiz-Zarzuela I, Halaihel N, Vendrell D, De Blas I, Múzquiz J (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355–360
Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MÁ, Esteban MÁ (2013) Changes in intestinal morphology and microbiota caused by dietary administration of inulin and Bacillus subtilis in gilthead sea bream (Sparus aurata L.) specimens. Fish Shellfish Immun 34:1063–1070
Flint HJ, Duncan SH, Scott KP, Louis P (2014) Links between diet, gut microbiota composition and gut metabolism. P Nutr Soc. doi: 10.1017/S0029665114001463
Abid A, Davies S, Waines P, Emery M, Castex M, Gioacchini G, Carnevali O, Bickerdike R, Romero J, Merrifield D (2013) Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity. Fish Shellfish Immun 35:1948–1956
Balcázar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz JL, Girones O (2008) Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 278:188–191
Burr G, Gatlin D (2005) Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. J World Aquacult Soc 36:425–236
Burrells C, Wiliams PD, Southgate PJ, Wadsworth SL (2001) Dietary nucleotides: a novel supplement in fish feeds 2. Effects on vaccination, salt water transfer, growth rates and physiology of Atlantic salmon (Salmo salar L.). Aquaculture 199:171–184
Moldal T, Løkka G, Wiik-Nielsen J, Austbø L, Torstensen BE, Rosenlund G, Dale OB, Kaldhusdal M, Koppang EO (2014) Substitution of dietary fish oil with plant oils is associated with shortened mid intestinal folds in Atlantic salmon (Salmo salar). BMC Vet Res 10:60
Ringø E, Løvmo L, Kristiansen M, Bakken Y, Salinas I, Myklebust R, Olsen RE, Mayhew TM (2009) Lactic acid bacteria vs. pathogens in the gastrointestinal tract of fish: a review. Aquac Res 41:451–467
Romarheim OH, Øverland M, Mydland LT, Skrede A, Landsverk T (2011) Bacteria grown on natural gas prevent soybean meal-induced enteritis in Atlantic salmon. J Nutr 141:124–130
Askarian F, Zhou Z, Olsen RE, Sperstad S, Ringø E (2012) Culturable autochthonous gut bacteria in Atlantic salmon (Salmo salar L.) fed diets with or without chitin. Characterisation by 16S rRNA gene sequencing, ability to produce enzymes and in vitro growth inhibition of four fish pathogens. Aquaculture 326:1–8
Korsnes K, Nicolaisen O, Skår CK, Nerland AH, Bergh Ø (2006) Bacteria in the gut of juvenile cod Gadus morhua fed live feed enriched with four different commercial diets. ICES J Mar Sci: J Conseil 263:296–301
Kotzamanis Y, Gisbert E, Gatesoupe F, Zambonino Infante J, Cahu C (2007) Effects of different dietary levels of fish protein hydrolysates on growth, digestive enzymes, gut microbiota, and resistance to Vibrio anguillarum in European sea bass (Dicentrarchus labrax) larvae. Comp Biochem Physiol 147:205–214
Landeira-Dabarca A, Sieiro C, Alvarez M (2013) Change in food ingestion induces rapid shifts in the diversity of microbiota associated with cutaneous mucus of Atlantic salmon Salmo salar. J Fish Biol 82:893–906
Ringø E, Olsen R (1999) The effect of diet on aerobic bacterial flora associated with intestine of Arctic charr (Salvelinus alpinus L.). J Appl Microbiol 86:22–28
Ringø E, Sperstad S, Myklebust R, Mayhew TM, Olsen RE (2006) The effect of dietary inulin on aerobic bacteria associated with hindgut of Arctic charr (Salvelinus alpinus L.). Aquac Res 37:891–897
Ringø E, Sperstad S, Myklebust R, Refstie S, Krogdahl Å (2006) Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.): the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 261:829–841
Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringo E, Krogdahl A (2007) Effects of dietary soya bean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Brit J Nutr 97:699–713
Bakke-McKellep A, Refstie S, Cyrino J, Bureau D, Kapoor B (2008) Alternative protein sources and digestive function alterations in teleost fishes. In: Cyrino JEP, Roubach R, Bureau D, Kapoor BG (eds) Feeding and digestive functions of fishes. Science Publishers, Enfield, NH, USA, pp 440–472
Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res 41:333–344
Sahlmann C, Sutherland BJ, Kortner TM, Koop BF, Krogdahl Å, Bakke AM (2013) Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. Fish Shellfish Immun 34:599–609
Refstie S, Glencross B, Landsverk T, Sørensen M, Lilleeng E, Hawkins W, Krogdahl Å (2006) Digestive function and intestinal integrity in Atlantic salmon (Salmo salar) fed kernel meals and protein concentrates made from yellow or narrow-leafed lupins. Aquaculture 261:1382–1395
Hartviksen M, Bakke AM, Vecino JG, Ringø E, Krogdahl Å (2014) Evaluation of the effect of commercially available plant and animal protein sources in diets for Atlantic salmon (Salmo salar L.): digestive and metabolic investigations. Fish Physiol Biochem 40:1621–1637
Turner JW Jr, Nemeth R, Rogers C (2003) Measurement of fecal glucocorticoids in parrotfishes to assess stress. Gen Comp Endocr 133:341–352
Niklasson L, Sundh H, Olsen RE, Jutfelt F, Skjødt K, Nilsen TO, Sundell KS (2014) Effects of cortisol on the intestinal mucosal immune response during cohabitant challenge with IPNV in Atlantic salmon (Salmo salar). PLoS One 9, e94288
Taylor RS, Muller WJ, Cook MT, Kube PD, Elliott NG (2009) Gill observations in Atlantic salmon (Salmo salar, L.) during repeated amoebic gill disease (AGD) field exposure and survival challenge. Aquaculture 290:1–8
Holben W, Williams P, Saarinen M, Särkilahti L, Apajalahti J (2002) Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microb Ecol 44:175–185
Hovda MB, Lunestad BT, Fontanillas R, Rosnes JT (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon (Salmo salar L.). Aquaculture 272:581–588
Soergel DA, Dey N, Knight R, Brenner SE (2012) Selection of primers for optimal taxonomic classification of environmental 16S rRNA gene sequences. ISME J 6:1440–1444
Dowd S, Callaway T, Wolcott R, Sun Y, McKeehan T, Hagevoort R, Edrington T (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125
Lanzén A, Jørgensen SL, Bengtsson MM, Jonassen I, Øvreås L, Urich T (2011) Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiol Ecol 77:577–589
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
Anderson MJ, Connell SD, Gillanders BM, Diebel CE, Blom WM, Saunders JE, Landers TJ (2005) Relationships between taxonomic resolution and spatial scales of multivariate variation. J Anim Ecol 74:636–646
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525
Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253
Spillman CM, Hobday AJ (2014) Dynamical seasonal ocean forecasts to aid salmon farm management in a climate hotspot. Climate Risk Management 1:25–38
Hunt S, Simpson T, Wright R (1982) Seasonal changes in the levels of 11‐oxotestosterone and testosterone in the serum of male salmon, Salmo salar L., and their relationship to growth and maturation cycle. J Fish Biol 20:105–119
Zarkasi KZ, Abell GC, Taylor RS, Neuman C, Hatje E, Tamplin ML, Katouli M, Bowman JP (2014) Pyrosequencing-based characterization of gastrointestinal bacteria of Atlantic salmon (Salmo salar L.) within a commercial mariculture system. J Appl Microbiol 117:18–27
Ratkowsky DA (2008) Tests for dispersion among macrofungal species assemblages. Australas Mycol 27:66–73
Krieg N (2011) Family IV. Porphyromonadaceae fam. nov. In Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB (editors), Bergey’s Manual of Systematic Bacteriology, second edition, vol. 4 (The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes). New York: Springer, 61-65
Dobson A, Cotter PD, Ross RP, Hill C (2012) Bacteriocin production: a probiotic trait? Appl Environ Microb 78:1–6
Beaz-Hidalgo R, Doce A, Balboa S, Barja JL, Romalde JL (2010) Aliivibrio finisterrensis sp. nov., isolated from Manila clam, Ruditapes philippinarum and emended description of the genus Aliivibrio. Int J Syst Evol Micr 60:223–228
Grammes F, Reveco FE, Romarheim OH, Landsverk T, Mydland LT, Øverland M (2013) Candida utilis and Chlorella vulgaris counteract intestinal inflammation in Atlantic salmon (Salmo salar L.). PLoS One 8, e83213
Tacchi L, Bickerdike R, Douglas A, Secombes CJ, Martin SA (2011) Transcriptomic responses to functional feeds in Atlantic salmon (Salmo salar). Fish Shellfish Immun 31:704–715
Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 19:1141–1152
Star B, Haverkamp TH, Jentoft S, Jakobsen KS (2013) Next generation sequencing shows high variation of the intestinal microbial species composition in Atlantic cod caught at a single location. BMC Microbiol 13:248
Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto JM, Kennedy S (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500:541–546
Ratkowsky D, Lowry R, McMeekin T, Stokes A, Chandler R (1983) Model for bacterial culture growth rate throughout the entire biokinetic temperature range. J Bacteriol 154:1222–1226
Soto W, Gutierrez J, Remmenga M, Nishiguchi M (2009) Salinity and temperature effects on physiological responses of Vibrio fischeri from diverse ecological niches. Microb Ecol 57:140–150
Chen WL, Oliver JD, Wong HC (2010) Adaptation of Vibrio vulnificus and an rpoS mutant to bile salts. Int J Food Microbiol 140:232–238
Neuman C, Hatje E, Zarkasi KZ, Smullen R, Bowman JP, Katouli M (2014) The effect of diet and environmental temperature on the faecal microbiota of farmed Tasmanian Atlantic Salmon (Salmo salar L.). Aquac Res. doi: 10.1111/are.12522
Hatje E, Neuman C, Stevenson H, Bowman JP, Katouli M (2014) Population dynamics of Vibrio and Pseudomonas species isolated from farmed Tasmanian Atlantic salmon (Salmo salar L.): a seasonal study. Microb Ecol 68:679–687
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65
Dantas G, Sommer MO, Degnan PH, Goodman AL (2013) Experimental approaches for defining functional roles of microbes in the human gut. Annu Rev Microbiol 67:459–475
Olsvik PA, Vikeså V, Lie KK, Hevrøy EM (2013) Transcriptional responses to temperature and low oxygen stress in Atlantic salmon studied with next-generation sequencing technology. BMC Genomics 14:817
Pédron T, Mulet C, Dauga C, Frangeul L, Chervaux C, Grompone G, Sansonetti PJ (2012) A crypt-specific core microbiota resides in the mouse colon. MBio 3:e00116–00112
Ivanov II, Littman DR (2010) Segmented filamentous bacteria take the stage. Mucosal Immunol 3:209–212
Fuhrman JA, Cram JA, Needham DM (2015) Marine microbial community dynamics and their ecological interpretation. Nat Rev Immunol 38:1690–1711
He M, Tian G, Semenov AM, van Bruggen AH (2012) Short-term fluctuations of sugar beet damping-off by Pythium ultimum in relation to changes in bacterial communities after organic amendments to two soils. Phytopathology 102:413–420
Van Diepeningen AD, De Vos OJ, Zelenev VV, Semenov AM, Van Bruggen AH (2005) DGGE fragments oscillate with or counter to fluctuations in cultivable bacteria along wheat roots. Microb Ecol 50:506–517
Zelenev V, Van Bruggen A, Semenov A (2005) Short-term wavelike dynamics of bacterial populations in response to nutrient input from fresh plant residues. Microb Ecol 49:83–93
Zelenev V, Van Bruggen A, Leffelaar P, Bloem J, Semenov A (2006) Oscillating dynamics of bacterial populations and their predators in response to fresh organic matter added to soil: the simulation model ‘BACWAVE-WEB’. Soil Biol Biochem 38:1690–1711
Acknowledgments
Thanks are extended to the Australian Seafood Cooperative Research Centre, Tassal Group and Skretting Australia for in-kind support and research funding (project 2011/701). The authors would also like to thank Dave Cameron for fish husbandry, Ben Maynard for assistance with research field sample preparation, Warren Muller for statistical advice on the cage trial and David Ratkowsky for statistical advice and discussions related to the experiments presented in this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Animal Ethics
All animal handling procedures were approved by the Tasmanian Department of Primary Industries, Parks, Water and Environment (DPIPWE) Animal Ethics Committee (Project 30/2009-10) under the guidelines of the Australian Code of Practice.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 60 kb)
Rights and permissions
About this article
Cite this article
Zarkasi, K.Z., Taylor, R.S., Abell, G.C.J. et al. Atlantic Salmon (Salmo salar L.) Gastrointestinal Microbial Community Dynamics in Relation to Digesta Properties and Diet. Microb Ecol 71, 589–603 (2016). https://doi.org/10.1007/s00248-015-0728-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-015-0728-y