Cite this paper:
XIA Mengjie, PEI Feng, MU Changkao, YE Yangfang, WANG Chunlin. Disruption of bacterial balance in the gut of Portunus trituberculatus induced by Vibrio alginolyticus infection[J]. HaiyangYuHuZhao, 2018, 36(5): 1891-1898

Disruption of bacterial balance in the gut of Portunus trituberculatus induced by Vibrio alginolyticus infection

XIA Mengjie1,2, PEI Feng1, MU Changkao1, YE Yangfang1, WANG Chunlin1
1 Key Laboratory of Applied Marine Biotechnology(Ningbo University), Ministry of Education, Ningbo 315211, China;
2 Collaborative Innovation Center for Zhejiang Marine High-Efficiency and Healthy Aquaculture, Ningbo 315211, China
Abstract:
Gut microbiota impacts the health of crustaceans. Vibrio alginolyticus is a main causative pathogen that induces the vibriosis in farmed swimming crabs, Portunus trituberculatus. However, it remains unknown whether gut bacteria perform functions during the progression of vibriosis. In this study, 16S rRNA gene amplicon sequencing was used to investigate temporal alteration of gut bacterial community in swimming crabs in response to 72-h V. alginolyticus challenge. Our results show that V. alginolyticus infection resulted in dynamic changes of bacterial community composition in swimming crabs. Such changes were highlighted by the overwhelming overabundance of Vibrio and a significant fluctuation in the gut bacteria including the bacteria with high relative abundance and especially those with low relative abundance. These findings reveal that crab vibriosis gradually develops with the infection time of V. alginolyticus and tightly relates to the dysbiosis of gut bacterial community structure. This work contributes to our appreciation of the importance of the balance of gut bacterial community structure in maintaining the health of crustaceans.
Key words:    Portunus trituberculatus|Vibrio alginolyticus|gut bacterial community composition|16S rRNA gene amplicon sequencing   
Received: 2017-06-02   Revised:
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Articles by XIA Mengjie
Articles by PEI Feng
Articles by MU Changkao
Articles by YE Yangfang
Articles by WANG Chunlin
References:
Bi K R, Zhang X J, Yan B L, Gao H, Gao X J, Sun J J. 2016.Isolation and molecular identification of Vibrio natriegens from diseased Portunus trituberculatus in China. Journal of the World Aquaculture Society, 47(6):854-861.
Brestoff J R, Artis D. 2013. Commensal bacteria at the interface of host metabolism and the immune system. Nature Immunology, 14(7):676-684.
Caporaso J G, Bittinger K, Bushman F D, DeSantis T Z, Andersen G L, Knight R. 2010b. 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. 2010a. QⅡME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5):335-336.
Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012.Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6(8):1 621-1 624.
Chen X B, Di P P, Wang H M, Li B L, Pan Y J, Yan S L, Wang Y J. 2015. Bacterial community associated with the intestinal tract of Chinese mitten crab (Eriocheir sinensis)farmed in Lake Tai, China. PLoS One, 10(4):e0123990.
Cheung M K, Yip H Y, Nong W, Law P T W, Chu K H, Kwan H S, Hui J H L. 2015. Rapid change of microbiota diversity in the gut but not the hepatopancreas during gonadal development of the new shrimp model Neocaridina denticulata. Marine Biotechnology, 17(6):811-819.
Cui Z X, Liu Y, Luan W S, Li Q Q, Wu D H, Wang S Y. 2010.Molecular cloning and characterization of a heat shock protein 70 gene in swimming crab (Portunus trituberculatus). Fish & Shellfish Immunology, 28(1):56-64.
De Schryver P, Vadstein O. 2014. Ecological theory as a foundation to control pathogenic invasion in aquaculture.The ISME Journal, 8:2 360-2 368.
Dicksved J, Halfvarson J, Rosenquist M, Järnerot G, Tysk C, Apajalahti J, Engstrand L, Jansson J K. 2008. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. The ISME Journal, 2:716-727.
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.
Gauthier M J. 1976. Alteromonas rubra sp. nov., a new marine antibiotic-producing bacterium. International Journal of Systematic Bacteriology, 26:459-466.
Kau A L, Ahern P P, Griffin N W, Goodman A L, Gordon J I. 2011. Human nutrition, the gut microbiome and the immune system. Nature, 474(7351):327-336.
Li M, Li C W, Wang J F, Song S Q. 2015. Molecular characterization and expression of a novel Toll gene from the swimming crab Portunus trituberculatus. Molecular Immunology, 67(2 Pt B):388-397.
Liu C H, Cheng W, Hsu J P, Chen J C. 2004. Vibrio alginolyticus infection in the white shrimp Litopenaeus vannamei confirmed by polymerase chain reaction and 16S rDNA sequencing. Diseases of Aquatic Organisms, 61(1-2):169-174.
Liu Q, Li H Y, Wang Q, Liu P, Dai F Y, Li J. 2007. Identification and phylogenetic analysis of a strain of Vibrio alginolyticus, a pathogen in Portunus trituberculatus with toothpaste disease. Marine Freshwater Research, 28(4):9-13. (in Chinese with English abstract)
Magoč T, Salzberg S L. 2011. FLASH:fast length adjustment of short reads to improve genome assemblies.Bioinformatics, 27(21):2 957-2 963.
Ohwada K, Tabor P S, Colwell R R, 1980. Species composition and barotolerance of gut microflora of deep-sea benthic macrofauna collected at various depths in the Atlantic ocean. Applied and Environmental Microbiology, 40(4):746-755.
Olmos J, Ochoa L, Paniagua-Michel J, Contreras R. 2011.Functional feed assessment on Litopenaeus vannamei using 100% fish meal replacement by soybean meal, high levels of complex carbohydrates and Bacillus probiotic strains. Marine Drugs, 9(6):1 119-1 132.
Qin J J, Li R Q, Raes J, Arumugam M, Burgdorf K S, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende D R, Li J H, Xu J M, Li S C, Li D F, Cao J J, Wang B, Liang H Q, Zheng H S, Xie Y L, Tap J, Lepage P, Bertalan M, Batto J M, Hansen T, Le Paslier D, Linneberg A, Nielsen H B, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H M, Yu C, Li S T, Jian M, Zhou Y, Li Y R, Zhang X Q, Li S G, Qin N, Yang H M, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, MetaHIT Consortium, Bork P, Ehrlich S D, Wang J. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464(7285):59-65.
Qin N, Yang F L, Li A, Prifti E, Chen Y F, Shao L, Guo J, Le Chatelier E, Yao J, Wu L J, Zhou J W, Ni S J, Liu L, Pons N, Batto J M, Kennedy S P, Leonard P, Yuan C H, Ding W C, Chen Y T, Hu X J, Zheng B W, Qian G R, Xu W, Ehrlich S D, Zheng S S, Li L J. 2014. Alterations of the human gut microbiome in liver cirrhosis. Nature, 513(7516):59-64.
Rungrassamee W, Klanchui A, Maibunkaew S, Karoonuthaisiri N. 2016. Bacterial dynamics in intestines of the black tiger shrimp and the Pacific white shrimp during Vibrio harveyi exposure. Journal of Invertebrate Pathology, 133:12-19.
Sampson T R, Debelius J W, Thron T, Janssen S, Shastri G G, Ilhan Z E, Challis C, Schretter C E, Rocha S, Gradinaru V, Chesselet M F, Keshavarzian A, Shannon K M, Krajmalnik-Brown R, Wittung-Stafshede P, Knight R, Mazmanian S K. 2016. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease. Cell, 167(6):1 469-1 480.e12.
Song X Y, Dai D, He X, Zhu S, Yao Y K, Gao H C, Wang J J, Qu F F, Qiu J, Wang H L, Li X X, Shen N, Qian Y C. 2015. Growth factor FGF2 cooperates with interleukin-17 to repair intestinal epithelial damage. Immunity, 43(3):488-501.
Tremaroli, V, Bäckhed, F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature, 489(7415):242-249.
Turnbaugh P J, Hamady M, Yatsunenko T, Cantarel B L, Duncan A, Ley R E, Sogin M L, Jones W J, Roe B A, Affourtit J P, Egholm M, Henrissat B, Heath A C, Knight R, Gordon J I. 2009. A core gut microbiome in obese and lean twins. Nature, 457(7228):480-484.
Wan X H, Shen H, Wang L B, Cheng Y X. 2011. Isolation and characterization of Vibrio metschnikovii causing infection in farmed Portunus trituberculatus in China. Aquaculture International, 19(2):351-359.
Wang G X, Huang Z R, Yuan M. 2007. Isolation and identification of the pathogen of milk disease cultured in swimming crab Portunus tritubercularus (portunidae). Journal of Northwest A & F University (Natural Science Edition), 35(6):29-33. (in Chinese with English abstract)
Wang Z N, Klipfell E, Bennett B J, Koeth R, Levison B S, DuGar B, Feldstein A E, Britt E B, Fu X M, Chung Y M, Wu Y P, Schauer P, Smith J D, Allayee H, Tang W H W, DiDonato J A, Lusis A J, Hazen S L. 2011. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature, 472(7341):57-63.
Wu H J, Sun L B, Li C B, Li Z Z, Zhang Z, Wen X B, Hu Z, Zhang Y L, Li S K. 2014. Enhancement of the immune response and protection against Vibrio parahaemolyticus by indigenous probiotic Bacillus strains in mud crab (Scylla paramamosain). Fish & Shellfish Immunology, 41:156-162.
Wu T, Zhang Z L, Cai C F, Ye Y T, Zhu J M, Li T. 2015. The effect of pectin and xylan on intestinal microflora structure of Chinese mitten crab. Genomics and Applied Biology, 34(4):745-753. (in Chinese with English abstract)
Xiong J B, Wang K, Wu J F, Qiuqian L, Yang K J, Qian Y X, Zhang D M. 2015. Changes in intestinal bacterial communities are closely associated with shrimp disease severity. Applied Microbiology and Biotechnology, 99(16):6 911-6 919.
Xiong J B, Zhu J Y, Dai W F, Dong C M, Qiu Q F, Li C H. 2017. Integrating gut microbiota immaturity and diseasediscriminatory taxa to diagnose the initiation and severity of shrimp disease. Environmental Microbiology, 19(4):1 490-1 501.
Yan B L, Qin G M, Bao Z H, Zhang X J, Bi K R, Qin L. 2010. Isolation and identification of Vibrio parahaemolyticus from diseased Portunus trituberculatus L. Marine Science Bulletin, 29(5):560-566. (in Chinese with English abstract)
Yang N, Zhang D F, Tao Z, Li M, Zhou S M, Wang G L. 2016. Identification of a novel class B scavenger receptor homologue in Portunus trituberculatus:molecular cloning and microbial ligand binding. Fish & Shellfish Immunology, 58:73-81.
Ye Y F, Xia M J, Mu C K, Li R H, Wang C L. 2016. Acute metabolic response of Portunus trituberculatus to Vibrio alginolyticus infection. Aquaculture, 463:201-208.
Yoshikawa K, Takadera T, Adachi K, Nishijima M, Sano H. 1997. Korormicin, a novel antibiotic specifically active against marine Gram-negative bacteria, produced by a marine bacterium. The Journal of Antibiotics, 50(11):949-953.
Zeng T L, Ye Y F, Mu C K, Wang K, Li R H, Wang C L. 2016. Gut microbiota and metabolic phenotype of Portunus trituberculatus. Chinese Journal of Analytical Chemistry, 44(12):1 867-1 873.
Zhang M L, Sun Y H, Chen L Q, Cai C F, Qiao F, Du Z Y, Li E C. 2016. Symbiotic bacteria in gills and guts of Chinese mitten crab (Eriocheir sinensis) differ from the free-living bacteria in water. PLoS One, 11(1):e0148135.
Zhang X J, Bai X S, Yan B L, Bi K R, Qin L. 2014. Vibrio harveyi as a causative agent of mass mortalities of megalopa in the seed production of swimming crab Portunus trituberculatus. Aquaculture International, 22(2):661-672.
Zhu J Y, Dai W F, Qiu Q F, Dong C M, Zhang J J, Xiong J B. 2016. Contrasting ecological processes and functional compositions between intestinal bacterial community in healthy and diseased shrimp. Microbial Ecology, 72(4):975-985.