Abstract
Partial substitutions of fish meal by 5, 15, or 25 % of Gracilaria cornea or Ulva rigida in experimental diets were evaluated to study their effects on biodiversity of intestinal microbiota composition in gilthead seabream (Sparus aurata) juveniles. The diets were offered to duplicate groups of 15 juvenile fish (14.0 ± 0.5 g) for 70 days, and at the end of the experiment the intestinal microbiota from four specimens of each treatment was analysed by denaturing gel gradient electrophoresis. Results showed that the substitution of fish meal by algae meal induced important modifications in the intestinal microbiota community, as a big reduction of the biodiversity when the highest percentage (25 %) of U. rigida was included. On the contrary, an increase on the number of species was detected when a 15 % of algae was included. Various Lactobacillus delbrueckii subspecies were selectively stimulated when G. cornea was included in the feed, and other bacterial species, such as those included in the Vibrio genus, were reduced.
Similar content being viewed by others
Abbreviations
- DGGE:
-
Denaturing gel gradient electrophoresis
- Fc:
-
Functional organization
- FCR:
-
Food conversion rate
- NCBI:
-
National Center for Biotechnology Information
- PBS:
-
Phosphate buffered saline
- PCR:
-
Polymerase chain reaction
- PER:
-
Protein efficiency rate
- R :
-
Specific richness
- Rr:
-
Range-weighted richness
- SGR:
-
Specific growth rate
- UPGMA:
-
Unweighted pair groups method arithmetic mean
References
Acerete L, Espinosa E, Josa A, Tort L (2009) Physiological response of hybrid striped bass subjected to Photobacterium damselae subsp piscicida. Aquaculture 298:16–23
Akayli T, Timur G, Albayrak G, Aydemir B (2010) Identification and genotyping of Vibrio ordalii: a comparison of different methods. Isr J Aquac Bamid 62:9–18
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignement search tool. J Mol Biol 215:403–410
Association of Analytical Chemists (2012) Official methods of analysis of official analytical chemists international, 19th edn. Association of Analytical Chemists (AOAC), Arlington
Ast JC, Cleenwerck I, Engelbeen K, Urbanczyk H, Thompson FL, De Vos P, Dunlap PV (2007) Photobacterium kishitanii sp nov., a luminous marine bacterium symbiotic with deep-sea fishes. Int J Syst Evol Microbiol 57:2073–2078
Austin B (2011) Taxonomy of bacterial fish pathogens. Vet Res 42:20
Bendiksen EA, Johnsen CA, Olsen HJ, Jobling M (2011) Sustainable aquafeeds: progress towards reduced reliance upon marine ingredients in diets for farmed Atlantic salmon (Salmo salar L.). Aquaculture 314:132–139
Brunvold L, Sandaa RA, Mikkelsen H, Welde E, Bleie H, Bergh O (2007) Characterization of bacterial communities associated with early stages of intensively reared cod (Gadus morhua) using denaturing gradient gel electrophoresis (DGGE). Aquaculture 272:319–327
Carnevali O, Zamponi MC, Sulpizio R, Rollo A, Nardi M, Orpianesi C, Silvi S, Caggiano M, Polzonetti AM, Cresci A (2004) Administration of probiotic strain to improve sea bream wellness during development. Aquac Int 12:377–386
Carnevali O, De Vivo L, Sulpizio R, Olivotto I, Silvi S, Cresci A (2006) Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax L.), with particular attention to IGF-1, myostatin and cortisol gene expression. Aquaculture 258:430–438
Cerezuela RM, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MA, Esteban MA (2013) Changes in intestinal morphology and microbiota caused by dietary administration of inulin and Bacillus subtilis in gilthead seabream (Sparus aurata L.) specimens. Fish Shellfish Immunol 34:1063–1070
Chabrillón M, Ouwenhand AC, Díaz-Rosales P, Arijo S, Martínez-Manzanares E, Balebona MC, Moriñigo MA (2006) Adhesion of lactic acid bacteria to mucus of farmed gilthead seabream, and interactions with fish pathogenic microorganisms. Bull Eur Assoc Fish Pathol 26:202–210
Dallaire V, Lessard P, Vandenberg G, de la Noüe J (2007) Effect of algal incorporation on growth, survival and carcass composition of rainbow trout (Oncorhynchus mykiss) fry. Bioresour Technol 98:1433–1439
De Paula Silva FC, Nicoli JR, Zambonino-Infante JL, Kaushik S, Gatesoupe FJ (2011) Influence of the diet on the microbial diversity of faecal and gastrointestinal contents in gilthead seabream (Sparus aurata) and intestinal contents in goldfish (Carassius auratus). FEMS Microbiol Ecol 78:285–296
Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, Güroy D, Davies SJ (2011) Microbial manipulations to improve fish health and production—a Mediterranean perspective. Fish Shellfish Immunol 30:1–16
Estruch G, Collado MC, Peñaranda DS, Tomás-Vidal A, Jover-Cerdá M, Pérez-Martínez G, Martínez-Llorens S (2015) Impact of fishmeal replacement in diets for gilthead seabream (Sparus aurata) on the gastrointestinal microbiota determined by pyrosequencing the 16S rRna gene. PLOS One. doi:10.1371/journal.pone.0136389
Fernández AS, Hashsham SA, Dollhopf SL, Raskin L, Glagoleva O, Dazzo FB, Hickey RF, Criddle CS, Tiedje JM (2000) Flexible community structure correlates with stable community function in methanogenic bioreactor communities perturbed by glucose. Appl Environ Microbiol 66:4058–4067
Floris R, Manca S, Fois N (2013) Microbial ecology of intestinal tract of gilthead seabream (Sparus aurata Linnaeus, 1758) from two coastal lagoons of Sardinia (Italy). Transit Water Bull 7:4–12
Food and Agriculture Organization of the United Nations (FAO) (2014) The state of world fisheries and aquaculture. FAO, Rome
Ganesan M, Thiruppathi S, Jha B (2006) Mariculture of Hypnea musciformis (Wulfen) Lamouroux in South east coast of India. Aquaculture 256:201–211
Ghanbari M, Kneifel W, Domig KJ (2015) A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448:464–475
Ghosh K, Roy M, Kar N, Ringø E (2010) Gastrointestinal bacteria in rohu, Labeo rohita (Actinopterygii: cypriniformes: cyprinidae): scanning electron microscopy and bacteriological study. Acta Ichthyol Piscat 40:129–135
Griffiths BS, Bonkowski M, Roy J, Ritz K (2001) Functional stability, substrate utilisation and biological indicators of soils following environmental impacts. Appl Soil Ecol 16:49–61
Heikkinen J, Vielma J, Kemiläinen O, Tiirola M, Eskelinen P, Kiuru T, Navia-Paldanius D, von Wright A (2006) Effects of soybean meal based diet on growth performance, gut histopathology and intestinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 261:259–268
Ibarz A, Padros F, Gallardo MA, Fernández-Borràs J, Blasco J, Ll Tort (2010) Low-temperature challenges to gilthead sea bream culture: review of cold-induced alterations and ‘Winter Syndrome’. Rev Fish Biol Fish 20:539–556
Kanchanopas-Barnette P, Labella A, Alonso CM, Manchado M, Castro D, Borrego JJ (2009) The First Isolation of Photobacterium damselae subsp damselae from Asian Seabass Lates calcarifer. Fish Pathol 44:47–50
Kim D, Austin B (2006) Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol 21:513–524
Kormas KA, Meziti A, Mente E, Frentzos A (2014) Dietary differences are reflected on the gut prokaryotic community structure of wild and commercially reared sea bream (Sparus aurata). Microbiol Open 3:718–728
Ludwig W, Strunk O, Westram R, Richter I, Meier H, Yadhukumar A, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371
Maidak BL, Cole JR, Parker CT Jr, Garrity GM, Larsen N, Li B, Lilburn TG, McCaughey MJ, Olsen GJ, Overbeek R, Pramanik S, Schmidt TM, Tiedje JM, Woese CR (1999) A new version of the RDP (Ribosomal Database Project). Nucleic Acids Res 27:171–173
Martín-Antonio B, Manchado M, Infante C, Zerolo R, Labella A, Alonso C, Borrego JJ (2007) Intestinal microbiota variation in Senegalese sole (Solea senegalensis) under different feeding regimes. Aquac Res 38:1213–1222
Martínez G, Shaw EM, Carrillo M, Zanuy S (1998) Protein salting-out method applied to genomic DNA isolation from fish whole blood. Biotechniques 24:138–139
Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol 10:1571–1581
Mata L, Silva J, Schuenoff A, Santos R (2006) The effects of light and temperature on the photosynthesis of the Asparagopsis armata tetrasporophyte (Falkenbergia rufolanosa), cultivated in tanks. Aquaculture 252:12–19
Mertens B, Boon N, Verstraete W (2005) Stereospecific effect of hexachlorocyclohexane on activity and structure of soil metanogenic communities. Environ Microbiol 7:660–669
Meziti A, Ramette A, Mente E, Kormas KA (2010) Temporal shifts of the Norway lobster (Nephrops norvegicus) gut bacterial communities. FEMS Microbiol Ecol 7:472–484
Miranda CD, Zemelman R (2002) Bacterial resistance to oxytetracycline in Chilean salmon farming. Aquaculture 212:31–47
Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes for 16S rRNA. Appl Environ Microbiol 59:695–700
Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14
Neugebauer KA, Gilliland SE (2005) Antagonistic action of lactobacillus delbrueckii ssp lactis RM-2 toward spoilage organisms in cottage cheese. J Dairy Sci 88:1335–1341
O’Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Mar Drugs 8:2028–2064
Pedersen K, Skall HF, Lassen-Nielsen AM, Nielsen TF, Henriksen NH, Olesen NJ (2008) Surveillance of health status on eight marine rainbow trout, Oncorhynchus mykiss (Walbaum), farms in Denmark in 2006. J Fish Dis 31:659–667
Pedersen AK, Turchini GM, Jahangard S, Ingram BA, Sherman CDH (2010) Effects of different dietary microalgae on survival, growth, settlement and fatty acid composition of blue mussel (Mytilus galloprovincialis) larvae. Aquaculture 309:115–124
Picchietti S, Mazzini M, Taddei AR, Renna R, Fausto AM, Mulero V, Carnevali O, Cresci A, Abelli L (2007) Effects of administration of probiotic strains on GALT of larval gilthead seabream: immunohistochemical and ultrastructural studies. Fish Shellfish Immunol 22:57–67
Picchietti S, Fausto AM, Randelli E, Carnevali O, Taddei AR, Buonocore F, Scapigliati G, Abelli L (2009) Early treatment with Lactobacillus delbrueckii strain induces an increase in intestinal T-cells and granulocytes and modulates immune-related genes of larval Dicentrarchus labrax (L.). Fish Shellfish Immunol 26:368–376
Preetha R, Jose S, Prathapan S, Vijayan KK, Jayaprakash NS, Philip R, Singh ISB (2010) An inhibitory compound produced by Pseudomonas with effectiveness on Vibrio harveyi. Aquac Res 41:1452–1461
Ramirez RF, Dixon BA (2003) Enzyme production by obligate intestinal anaerobic bacteria isolated from Oscars (Astronotus ocellatus), angelfish (Pterophyllum scalare) and southern flounder (Paralichthys lethostigma). Aquaculture 227:417–426
Ringø E, Myklebust R, Mayhew TM, Olsen RE (2007) Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268:251–264
Ringø E, Løvmo L, Kristiansen M, Bakken Y, Salinas I, Myklebust R, Olsen R, Mayhew TM (2010) Lactic acid bacteria vs. pathogens in the gastrointestinal tract of fish: a review. Aquac Res 41:451–467
Rombout JH, Abelli L, Picchietti S, Scapigliati G, Kiron V (2011) Teleost intestinal immunology. Fish Shellfish Immunol 31:616–626
Sáenz de Rodrigáñez MA, Díaz-Rosales P, Chabrillón M, Smidt H, Arijo S, León-Rubio JM, Alarcón FJ, Balebona MC, Moriñigo MA, Cara JB, Moyano FJ (2009) Effect of dietary administration of probiotics on growth and digestive tract of Senegalese sole (Solea senegalensis, Kaup 1858). Aquac Nutr 15:177–185
Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Salgado-Miranda C, Palomares E, Jurado M, Marín A, Vega F, Soriano-Vargas E (2010) Isolation and distribution of bacterial flora in farmed rainbow trout from Mexico. J Aquat Anim Health 22:244–247
Salinas I, Cuesta A, Esteban MA, Meseguer J (2005) Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish Shellfish Immunol 19:67–77
Sekirov I, Finlay BB (2009) The role of the intestinal microbiota in enteric infection. J Physiol 587:4159–4167
Shao JP, Tian X, Ying B (2006) Dynamic changes of total bacteria and Vibrio in an integrated seaweed-abalone culture system. Aquaculture 252:289–297
Stadtlander T, Khalil WKB, Focken U, Becker K (2013) Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth, feed utilization and metabolism in intensively fed Nile tilapia Oreochromis niloticus (L.). Aquac Nutr 19:64–73
Suzer C, Coban D, Kamaci HO, Saka S, Firat K, Otgucuoglu O, Küçüksari H (2008) Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture 280:140–145
Taboada C, Millan R, Miguez I (2011) Evaluation of the marine alga Ulva rigida as a food supplement: effect of intake on intestinal, hepatic, and renal enzyme activities in rats. J Med Food 14:161–166
Tapia-Paniagua ST, Chabrillón M, Díaz-Rosales P, García de la Banda I, Lobo C, Balebona MC, Moriñigo MA (2010) Intestinal microbiota diversity of the flat fish Solea senegalensis (Kaup, 1858) following probiotic administration. Microbiol Ecol 60:310–319
Tapia-Paniagua ST, Vidal S, Lobo C, Prieto-Alamo MJ, Jurado J, Cordero H, Cerezuela R, García de la Banda I, Esteban MA, Balebona MC, Moriñigo MA (2014) The treatment with the probiotic Shewanella putrefaciens Pdp11 of specimens of Solea senegalensis exposed to high stocking densities to enhance their resistance to disease. Fish Shellfish Immunol 41:209–221
Tkavc R, Ausec L, Oren A, Gunde-Cimerman N (2011) Bacteria associated with Artemia spp alon the salinity of the solar salterns at Eilat (Israel). FEMS Microbiol Ecol 77:310–321
Trigui M, Gasmi L, Zouari I, Tounsi S (2013) Seasonal variation in phenolifc composition, antibacterial and antioxidant activities of Ulva rigida (Chlorophyta) and assessment of antiacetylcholineterase potential. J Appl Phycol 25:319–328
Vázquez JA, González MP, Murado MA (2005) Effects of lactic acid bacteria cultures on pathogenic microbiota from fish. Aquaculture 245:149–161
Vidanarachchi JK, Elangovan AV, Mikkelsen LL, Choct M, Iji PA (2010) Effect of some plant extracts on growth performance intestinal morphology, microflora composition and activity in broiler chickens. Anim Prod Sci 50:880–889
Viera MP, Gómez Pinchetti JLG, de Vicose GC, Bilbao A, Suárez S, Haroun RJ, Izquierdo MS (2005) Suitability of three red macroalgae as a feed for the abalone Haliotis tuberculata coccinea Reeve. Aquaculture 248:75–82
Vizcaíno AJ, Mendes SI, Varela JL, Ruiz-Jarabo I, Rico R, López-Figueroa F, Abdala R, Moriñigo MA, Mancera JM, Alarcón FJ (2015) Growth, tissue metabolites and digestive functionality in Sparus aurata juveniles fed different levels of macroalgae, Gracilaria cornea and Ulva rigida. Aquac Res. doi:10.1111/are.12774
Walker AB, Fournier HR, Neffus CD, Nardi GC, Berlinsky DL (2009) Partial replacement of fish meal with laver Porphyra spp. in diets for Atlantic cod. N Am J Aquac 71:39–45
Weinbauer MG, Bonilla-Findji O, Chan AM, Dolan JR, Short SM, Simek K, Wilheim SW, Suttle CA (2011) Synechococcus growth in the ocean may depend on the lysis of heterotrophic bacteria. J Plankton Res 33:1465–1476
Wittebolle L, Vervaeren H, Verstraete W, Boon N (2008) Quantifying community dynamics of nitrifiers in functionally stable reactors. Appl Environ Microbiol 74:286–293
Yin LJ (2009) Development of the prebiotics from lactic acid bacteria fermented algae hydrolysates and evaluation of their functionality. New Biotechnol. 25(Suppl 1):S116–S117
Yoon-Dong P, Keun SB, Chi NS, Kyung SB, Sanggoo K, Jongsik C (2006) Photobacterium ganghwense sp, nov, a halophilic bacterium isolated from sea water. Int J Syst Evol Microbiol 56:745–749
Zhang WW, Hu YH, Wang HL, Sun L (2009) Identification and characterization of a virulence-associated protease from a pathogenic Pseudomonas fluorescens strain. Vet Microbiol 139:183–188
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rico, R.M., Tejedor-Junco, M.T., Tapia-Paniagua, S.T. et al. Influence of the dietary inclusion of Gracilaria cornea and Ulva rigida on the biodiversity of the intestinal microbiota of Sparus aurata juveniles. Aquacult Int 24, 965–984 (2016). https://doi.org/10.1007/s10499-015-9964-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-015-9964-x