Abstract
Gut microbiota plays a crucial importance in their host. Disturbance of the microbial structure and function is known to be associated with inflammatory intestinal disorders. Enteritis is a significant cause of high mortality in fish species, including grass carp (Ctenopharyngodon idellus). Study regarding the association between microbial alternations and enteritis in grass carp is still absent. In this study, changes in the gut microbiota of grass carp suffering from enteritis were investigated using NGS-based 16S rRNA sequencing. Six healthy and ten abnormal fish (showing reddening anus, red odiferous fluid accumulating in the abdominal capacity, and flatulence and haemorrhage in the intestine) were collected from a fish farm in Huanggang Fisheries Institute (Hubei, China). Our results revealed that the diversity, structure, and function of gut microbiota were significantly different between diseased and healthy fish (P < 0.05). Particularly, members of the genera Dechloromonas, Methylocaldum, Planctomyces, Rhodobacter, Caulobacter, Flavobacterium, and Pseudomonas were significantly increased in diseased fish compared with that in healthy fish (P < 0.05). Predicted function indicated that microbiota significantly changed the specific metabolic pathways (related to amino acid metabolism, xenobiotics biodegradation and metabolism, and carbohydrate metabolism) in diseased fish (P < 0.05). Taken together, our findings point out the association between changes of the gut microbiota and enteritis in grass carp, which provide basic information useful for diagnoses, prevention, and treatment of intestinal diseases occurring in cultured fish.
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References
Baker G, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555. https://doi.org/10.1016/j.mimet.2003.08.009
Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ (2015) Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis 26:26191. https://doi.org/10.3402/mehd.v26.26191
Chen W, Liu F, Ling Z, Tong X, Xiang C (2012) Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS ONE 7:e39743
Cudmore B, Mandrak NE (2004) Biological synopsis of grass carp (Ctenopharyngodon idella). Can Manuscr Rep Fish Aquat Sci 2705:v+44
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
FAO (2014) FAO yearbook: fishery and aquaculture statistics. FAO, Rome
FBCAD (2014) China fishery statistical yearbook. China Agriculture Press, Bejing
Ganguly S, Prasad A (2012) Microflora in fish digestive tract plays significant role in digestion and metabolism. Rev Fish Biol Fish 22:11–16
Gao Z, Guo B, Gao R, Zhu Q, Qin H (2015) Microbiota disbiosis is associated with colorectal cancer. Front Microbiol 6:20. https://doi.org/10.3389/fmicb.2015.00020
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9
Hong Y et al (2015) Growth, digestive and absorptive capacity and antioxidant status in intestine and hepatopancreas of sub-adult grass carp Ctenopharyngodon idella fed graded levels of dietary threonine. JASB 6:34
Langille MGI et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Li Q, Wang C, Tang C, Li N, Li J (2012) Molecular-phylogenetic characterization of the microbiota in ulcerated and non-ulcerated regions in the patients with Crohn’s disease. PLoS ONE 7:e34939
Li F, Wang K, Luo W, Huang L, Lin Q (2015) Comparison of the intestinal bacterial flora in healthy and intestinal-diseased seahorses Hippocampus trimaculatus, Hippocampus erectus, and Hippocampus spinosissimus. JWAS 46:263–272
Li T et al (2016) Alterations of the gut microbiome of largemouth bronze gudgeon (Coreius guichenoti) suffering from furunculosis. Sci Rep 6:30606
Lozupone C, Hamady M, Knight R (2006) UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinf 7:371. https://doi.org/10.1186/1471-2105-7-371
Luan C et al (2015) Dysbiosis of fungal microbiota in the intestinal mucosa of patients with colorectal adenomas. Sci Rep 5:7980
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Mao D-P, Zhou Q, Chen C-Y, Quan Z-X (2012) Coverage evaluation of universal bacterial primers using the metagenomic datasets. BMC Microbiol 12:66. https://doi.org/10.1186/1471-2180-12-66
NACA (1989) Integrated fish farming in China vol NACA technical manual 7. Integrated fish farming. A world food day publication of the Network of Aquaculture Centres in Asia and the Pacific, Bangkok
Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquacult Res 41:1553–1573. https://doi.org/10.1111/j.1365-2109.2010.02546.x
Nie D-S, Pan J-P (1985) Diseases of grass carp (Ctenopharyngodon idellus Valenciennes, 1844) in China, a review from 1953 to 1983. Fish Pathol 20:323–330
Nie D, Wang J (1999) Biology and diseases of grass carp. Science press, Beijing
Pei YY, Huang R, Li YM, Liao LJ, Zhu ZY, Wang YP (2015) Characterizations of four toll-like receptor 4s in grass carp Ctenopharyngodon idellus and their response to grass carp reovirus infection and lipopolysaccharide stimulation. J Fish Biol 86:1098–1108
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. https://doi.org/10.1038/mi.2010.12
Pond MJ, Stone DM, Alderman DJ (2006) Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Aquaculture 261:194–203. https://doi.org/10.1016/j.aquaculture.2006.06.037
Ray A, Ghosh K, Ringø E (2012) Enzyme-producing bacteria isolated from fish gut: a review. Aquacult Nutr 18:465–492
Roy T, Mondal S, Ray AK (2009) Phytase-producing bacteria in the digestive tracts of some freshwater fish. Aquacult Res 40:344–353. https://doi.org/10.1111/j.1365-2109.2008.02100.x
Saha S, Roy RN, Sen SK, Ray AK (2006) Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes). Aquacult Res 37:380–388. https://doi.org/10.1111/j.1365-2109.2006.01442.x
She R et al (2017) Changes in the intestinal microbiota of gibel carp (Carassius gibelio) associated with cyprinid herpesvirus 2 (CyHV-2) infection. Curr Microbiol 74:1130–1136. https://doi.org/10.1007/s00284-017-1294-y
Shin N-R, Whon TW, Bae J-W (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503. https://doi.org/10.1016/j.tibtech.2015.06.011
Sokol H et al (2006) Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm Bowel Dis 12:106–111
Sokol H et al. (2016) Fungal microbiota dysbiosis in IBD. Gut. https://doi.org/10.1136/gutjnl-2015-310746
Song X, Zhao J, Bo Y, Liu Z, Wu K, Gong C (2014) Aeromonas hydrophila induces intestinal inflammation in grass carp (Ctenopharyngodon idella): an experimental model. Aquaculture 434:171–178
Sugita H, Miyajima C, Deguchi Y (1991) The vitamin B12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 92:267–276
Tran NT, Wang GT, Wu SG (2017) A review of intestinal microbes in grass carp Ctenopharyngodon idellus (Valenciennes). Aquacult Res 48:3287–3297. https://doi.org/10.1111/are.13367
Wang C, Sun G, Li S, Li X, Liu Y (2017) Intestinal microbiota of healthy and unhealthy Atlantic salmon Salmo salar L. in a recirculating aquaculture system. Chinese J Oceanol Limnol. https://doi.org/10.1007/s00343-017-6203-5
Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS ONE 7:e30440. https://doi.org/10.1371/journal.pone.0030440
Xia J et al (2014) The intestinal microbiome of fish under starvation. BMC Genom 15:266. https://doi.org/10.1186/1471-2164-15-266
Yang Y, Jobin C (2014) Microbial imbalance and intestinal pathologies: connections and contributions. Dis Model Mech 7:1131–1142
Yang Q et al (2017) Structure and function of the fecal microbiota in diarrheic neonatal piglets. Front Microbiol 8:502. https://doi.org/10.3389/fmicb.2017.00502
Zheng H et al (2016) Altered gut microbiota composition associated with eczema in infants. PLoS ONE 11:e0166026
Zhu Q et al (2014) Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS ONE 9:e90849. https://doi.org/10.1371/journal.pone.0090849
Acknowledgements
The first author, Ngoc Tuan Tran, would like to thank Chinese Academy of Sciences (CAS) for providing a Postdoctoral Fellowship under the CAS President’s International Fellowship Initiative (PIFI). This work was supported by National Natural Science Foundation of China (No. 31372571 and No. 31272706) and the earmarked fund for China Agriculture Research System (No. CARS-45-15).
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Tran, N.T., Zhang, J., Xiong, F. et al. Altered gut microbiota associated with intestinal disease in grass carp (Ctenopharyngodon idellus). World J Microbiol Biotechnol 34, 71 (2018). https://doi.org/10.1007/s11274-018-2447-2
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DOI: https://doi.org/10.1007/s11274-018-2447-2