Effects of dietary supplementation of <i>Ulva pertusa</i> and nonstarch polysaccharide enzymes on gut microbiota of <i>Siganus canaliculatus</i> -- Journal of Oceanology and Limnology,2018,36(2):438-449

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	ZHANG Xinxu, WU Huijuan, LI Zhongzhen, LI Yuanyou, WANG Shuqi, ZHU Dashi, WEN Xiaobo, LI Shengkang. Effects of dietary supplementation of Ulva pertusa and nonstarch polysaccharide enzymes on gut microbiota of Siganus canaliculatus[J]. Journal of Oceanology and Limnology, 2018, 36(2): 438-449

Effects of dietary supplementation of Ulva pertusa and nonstarch polysaccharide enzymes on gut microbiota of Siganus canaliculatus

ZHANG Xinxu^1,2, WU Huijuan^1,2, LI Zhongzhen^1,2, LI Yuanyou^1,2, WANG Shuqi^1,2, ZHU Dashi^1,2, WEN Xiaobo^1,2, LI Shengkang^1,2

1 Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou 515063, China;
2 Marine Biology Institute, Shantou University, Shantou 515063, China

Abstract:

Fishes represent the highest diversity of vertebrates; however, our understanding of the compositions and functions of their gut microbiota is limited. In this study, we provided the first insight into the gut microbiota of the herbivorous fish Siganus canaliculatus by using three molecular ecology techniques based on the 16S rRNA genes (denaturing gradient gel electrophoresis, clone library construction, and highthroughput Illumina sequencing), and the Illumina sequencing technique is suggested here due to its higher overall coverage of the total 16S rRNA genes. A core gut microbiota of 29 bacterial groups, covering >99.9% of the total bacterial community, was found to be dominated by Proteobacteria and Firmicutes in fish fed three different diets with/without the supplementation of Ulva pertusa and non-starch polysaccharide (NSP) enzymes (cellulase, xylanase, and β-glucanase). Diverse potential NSP-degrading bacteria and probiotics (e.g., Ruminococcus, Clostridium and Lachnospiraceae) were detected in the intestine of the fish fed U. pertusa, suggesting that these microorganisms likely participated in the degradation of NSPs derived from U. pertusa. This study supports our previous conclusion that U. pertusa-based diets are suitable for the production of S. canaliculatus with lower costs without compromising quality.

Key words: aquaculture|gut microbiota|Siganus canaliculatus|16S rRNA gene|Ulva pertusa

Received: 2016-09-19 Revised:

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References:
Ai Q H, Mai K S, Zhang W B, Xu W, Tan B P, Zhang C X, Li H T. 2007. Effects of exogenous enzymes (phytase, nonstarch polysaccharide enzyme) in diets on growth, feed utilization, nitrogen and phosphorus excretion of Japanese seabass, Lateolabrax japonicus. Comp. Biochem. Physiol.A Mol. Integr. Physiol., 147(2):502-508.
Allan G L, Parkinson S, Booth M A, Stone D A J, Rowland S J, Frances J, Warner-Smith R. 2000. Replacement of fish meal in diets for Australian silver perch, Bidyanus bidyanus:I. Digestibility of alternative ingredients.Aquaculture, 186(3-4):293-310.
Almirall M, Francesch M, Perez-Vendrell A M, Brufau J, Esteve-Garcia E. 1995. The differences in intestinal viscosity produced by barley and β-glucanase alter digesta enzyme activities and ileal nutrient digestibilities more in broiler chicks than in cocks. J. Nutr., 125(4):947-955.
Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990.Basic local alignment search tool. J. Mol. Biol., 215(3):403-410.
Attene-Ramos M S, Wagner E D, Plewa M J, Gaskins H R. 2006. Evidence that hydrogen sulfide is a genotoxic agent.Mol. Cancer Res., 4(1):9-14.
Caporaso J G, Bittinger K, Bushman F D, DeSantis T Z, Andersen G L, Knight R. 2010a. PyNAST:a flexible tool for aligning sequences to a template alignment.Bioinformatics, 26(2):266-267.
Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010b. QⅡME allows analysis of high-throughput community sequencing data. Nat.Methods, 7(5):335-336.
Choct M. 1997. Feed non-starch polysaccharides:chemical structures and nutritional significance. Feed Milling Int., (June):13-26.
Clements K D, Pasch I B Y, Moran D, Turner S J. 2007.Clostridia dominate 16S rRNA gene libraries prepared from the hindgut of temperate marine herbivorous fishes.Mar. Biol., 150(6):1 431-1 440.
Cruaud P, Vigneron A, Lucchetti-Miganeh C, Ciron P E, Godfroy A, Cambon-Bonavita M A. 2014. Influence of DNA extraction method, 16S rRNA targeted hypervariable regions, and sample origin on microbial diversity detected by 454 pyrosequencing in marine chemosynthetic ecosystems. Appl. Environ. Microbiol., 80(15):4 626-4 639.
David L A, Maurice C F, Carmody R N, Gootenberg D B, Button J E, Wolfe B E, Ling A V, Devlin A S, Varma Y, Fischbach M A, Biddinger S B, Dutton R J, Turnbaugh P J. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505(7484):559-563.
DeSantis T Z, Hugenholtz P, Larsen N, Rojas M, Brodie E L, Keller K, Huber T, Dalevi D, Hu P, Andersen G L. 2006.Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ.Microbiol., 72(7):5 069-5 072.
Durbán A, Abellán J J, Jiménez-Hernández N, Latorre A, Moya A. 2012. Daily follow-up of bacterial communities in the human gut reveals stable composition and hostspecific patterns of interaction. FEMS Microbiol. Ecol., 81(2):427-437.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011.UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16):2 194-2 200.
Edgar R C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19):2 460-2 461.
Flint H J, Bayer E A, Rincon M T, Lamed R, White B A. 2008.Polysaccharide utilization by gut bacteria:potential for new insights from genomic analysis. Nat. Rev. Microbiol., 6(2):121-131.
Gómez G D, Balcázar J L. 2008. A review on the interactions between gut microbiota and innate immunity of fish.FEMS Immunol. Med. Microbiol., 52(2):145-154.
Güroy B, Ergün S, Merrifield D L, Güroy D. 2013. Effect of autoclaved Ulva meal on growth performance, nutrient utilization and fatty acid profile of rainbow trout, Oncorhynchus mykiss. Aquacult. Int., 21(3):605-615.
Hammer O, Harper D A T, Ryan P. 2001. PAST:paleontological statistics software package for education and data analysis.Palaeontologia Electronica, 4(1):1-9.
Heidelberg J F, Seshadri R, Haveman S A, Hemme C L, Paulsen I T, Kolonay J F, Eisen J A, Ward N, Methe B, Brinkac L M, Daugherty S C, Deboy R T, Dodson R J, Durkin A S, Madupu R, Nelson W C, Sullivan S A, Fouts D, Haft D H, Selengut J, Peterson J D, Davidsen T M, Zafar N, Zhou L W, Radune D, Dimitrov G, Hance M, Tran K, Khouri H, Gill J, Utterback T R, Feldblyum T V, Wall J D, Voordouw G, Fraser C M. 2004. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat. Biotechnol., 22(5):554-559.
Kato S, Haruta S, Cui Z J, Ishii M, Yokota A, Igarashi Y. 2004.Clostridium straminisolvens sp. nov., a moderately thermophilic, aerotolerant and cellulolytic bacterium isolated from a cellulose-degrading bacterial community.Int. J. Syst. Evol. Microbiol., 54(6):2 043-2 047.
Kong Y H, Teather R, Forster R. 2010. Composition, spatial distribution, and diversity of the bacterial communities in the rumen of cows fed different forages. FEMS Microbiol.Ecol., 74(3):612-622.
Kumar S, Sahu N P, Pal A K, Choudhury D, Mukherjee S C. 2006. Studies on digestibility and digestive enzyme activities in Labeo rohita (Hamilton) juveniles:effect of microbial α-amylase supplementation in non-gelatinized or gelatinized corn-based diet at two protein levels. Fish Physiol. Biochem., 32(3):209-220.
Kuz'mina V V. 1996. Influence of age on digestive enzyme activity in some freshwater teleosts. Aquaculture, 148(1):25-37.
Leenhouwers J I, Ortega R C, Verreth J A J, Schrama J W. 2007. Digesta characteristics in relation to nutrient digestibility and mineral absorption in Nile tilapia (Oreochromis niloticus L.) fed cereal grains of increasing viscosity. Aquaculture, 273(4):556-565.
Ley R E, Lozupone C A, Hamady M, Knight R, Gordon J I. 2008. Worlds within worlds:evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol., 6(10):776-788.
Li Q, Wang S Q, You C H, Li Y Y. 2013. Comparison of three Non-starch polysaccharide enzymes on the in vitro digestibility of several kinds of marine algae. Siliao Gongye, 34(22):37-41. (in Chinese)
Li S, Sun L, Wu H, Hu Z, Liu W, Li Y, Wen X. 2012. The intestinal microbial diversity in mud crab (Scylla paramamosain) as determined by PCR-DGGE and clone library analysis. J. Appl. Microbiol., 113(6):1 341-1 351.
Li Y Y, Hu C B, Zheng Y J, Xia X A, Xu W J, Wang S Q, Chen W Z, Sun Z W, Huang J H. 2008. The effects of dietary fatty acids on liver fatty acid composition and △6-desaturase expression differ with ambient salinities in Siganus canaliculatus. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 151(2):183-190.
Nayak S K. 2010. Role of gastrointestinal microbiota in fish.Aquacult. Res., 41(11):1 553-1 573.
O'Connell J M, Sweeney T, Callan J J, O'Doherty J V. 2005.The effect of cereal type and exogenous enzyme supplementation in pig diets on nutrient digestibility, intestinal microflora, volatile fatty acid concentration and manure ammonia emissions from finisher pigs. Animal Science, 81(3):357-364.
Pankratov T A, Dedysh S N, Zavarzin G A. 2006. The leading role of actinobacteria in aerobic cellulose degradation in Sphagnum peat bogs. Dokl. Biol. Sci., 410(1):428-430.
Pérez-Sánchez T, Ruiz-Zarzuela I, de Blas I, Balcázar J L. 2014. Probiotics in aquaculture:a current assessment.Rev. Aquacult., 6(3):133-146.
Pinto A J, Raskin L. 2012. PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets.PLoS One, 7(8):e43093.
Price M N, Dehal P S, Arkin A P. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One, 5(3):e9490.
R Core Team. 2015. R:a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.r-project.org/.
Rawls J F, Samuel B S, Gordon J I. 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. U. S. A., 101(13):4 596-4 601.
Refstie S, Svihus B, Shearer K D, Storebakken T. 1999.Nutrient digestibility in Atlantic salmon and broiler chickens related to viscosity and non-starch polysaccharide content in different soyabean products. Anim. Feed Sci.Technol., 79(4):331-345.
Ringø E, Strøm E, Tabachek J A. 1995. Intestinal microflora of salmonids:a review. Aquacult. Res., 26(10):773-789.
Roeselers G, Mittge E K, Stephens W Z, Parichy D M, Cavanaugh C M, Guillemin K, Rawls J F. 2011. Evidence for a core gut microbiota in the zebrafish. ISME J., 5(10):1 595-1 608.
Saha S, Roy R N, Sen S K, Ray A K. 2006. Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes). Aquacult. Res., 37(4):380-388.
Salonen A, Lahti L, Salojärvi J, Holtrop G, Korpela K, Duncan S H, Date P, Farquharson F, Johnstone A M, Lobley G E, Louis P, Flint H J, de Vos W M. 2014. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J., 8(11):2 218-2 230.
Shade A, Handelsman J. 2012. Beyond the Venn diagram:the hunt for a core microbiome. Environ. Microbiol., 14(1):4-12.
Sijpesteijn A K. 1951. On ruminococcus flavefaciens, a cellulose-decomposing bacterium from the rumen of sheep and cattle. J. Gen. Microbiol., 5:869-879.
Sinha A K, Kumar V, Makkar H P S, De Boeck G, Becker K. 2011. Non-starch polysaccharides and their role in fish nutrition-A review. Food Chem., 127(4):1 409-1 426.
Storebakken T, Kvien I S, Shearer K D, Grisdale-Helland B, Helland S J. 1999. Estimation of gastrointestinal evacuation rate in Atlantic salmon (Salmo salar) using inert markers and collection of faeces by sieving:evacuation of diets with fish meal, soybean meal or bacterial meal. Aquaculture, 172(3-4):291-299.
Sullam K E, Essinger S D, Lozupone C A, O'Connor M P, Rosen G L, Knight R O B, Kilham S S, Russell J A. 2012.Environmental and ecological factors that shape the gut bacterial communities of fish:a meta-analysis. Mol. Ecol., 21(13):3 363-3 378.
Teske A, Sørensen K B. 2008. Uncultured archaea in deep marine subsurface sediments:have we caught them all?ISME J., 2(1):3-18.
Tolentino-Pablico G, Bailly N, Froese R, Elloran C. 2008.Seaweeds preferred by herbivorous fishes. J. Appl.Phycol., 20(5):933-938.
Van Soest P J. 1994. Nutritional Ecology of the Ruminant. 2nd edn. Cornell University Press, Ithaca.
Větrovský T, Baldrian P. 2013. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One, 8(2):e57923.
von Westernhagen H. 1973. The natural food of the rabbitfish Siganus oramin and S. striolata. Mar. Biol., 22(4):367-370.
Wang S Q, Xu S D, Wu Q Y, Zhang L, Zhang T, You C H, Zheng H P, Li Y Y. 2010. Optimal levels of protein and lipid in diets for rabbitfish Siganus canaliculatus juvenile.Marine Sciences, 34(11):18-22. (in Chinese with English abstract)
White W L, Coveny A H, Robertson J, Clements K D. 2010.Utilisation of mannitol by temperate marine herbivorous fishes. J. Exp. Mar. Biol. Ecol., 391(1-2):50-56.
Wong S, Waldrop T, Summerfelt S, Davidson J, Barrows F, Kenney P B, Welch T, Wiens G D, Snekvik K, Rawls J F, Good C. 2013. Aquacultured rainbow trout (Oncorhynchus mykiss) possess a large core intestinal microbiota that is resistant to variation in diet and rearing density. Appl.Environ. Microbiol., 79(16):4 974-4 984.
Wu S G, Wang G T, Angert E R, Wang W W, Li W X, Zou H. 2012. Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One, 7(2):e30440.
Xu S D, Zhang L, Wu Q Y, Liu X B, Wang S Q, You C H, Li Y Y. 2011. Evaluation of dried seaweed Gracilaria lemaneiformis as an ingredient in diets for teleost fish Siganus canaliculatus. Aquacult. Int., 19(5):1 007-1 018.
Ye L, Amberg J, Chapman D, Gaikowski M, Liu W T. 2014.Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J., 8(3):541-551.
You C H, Zeng F G, Wang S Q, Li Y Y. 2014a. Preference of the herbivorous marine teleost Siganus canaliculatus for different macroalgae. J. Ocean Univ. China, 13(3):516-522.
You C H, Zhang W T, Wang S Q, Cheng C H K, Li Y Y. 2014b.Evaluation of green alga Ulva pertusa as a dietary ingredient for rabbitfish Siganus canaliculatus juveniles.J. J. Aquacul. Res., 1(1):005.
Zhang M L, Sun Y H, Liu Y K, Qiao F, Chen L Q, Liu W T, Du Z Y, Li E C. 2016. Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture, 454:72-80.
Zhang W. 2012. Primary Study on the Utilization of MacroAlga Ulva Pertusa as Dietary Ingredient. Shantou University. (in Chinese with English abstract)