Disruption of bacterial balance in the gut of Portunus trituberculatus induced by Vibrio alginolyticus infection
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摘要
A bstract Gut microbiota impacts the health of crustaceans. V ibrio 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, 16 SrRNA 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 V ibrio 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.
A bstract Gut microbiota impacts the health of crustaceans. V ibrio 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, 16 SrRNA 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 V ibrio 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.
A bstract Gut microbiota impacts the health of crustaceans. V ibrio 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, 16 SrRNA 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 V ibrio 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.
引文
Bi K R,Zhang X J,Yan B L,Gao H,Gao X J,Sun J J.2016.Isolation and molecular identifi cation of Vibrio natriegens from diseased Portunus trituberculatus in China.J ournal of the World Aquacult ure Soc iety,47(6):854-861.
Brestoff J R,Artis D.2013.Commensal bacteria at the interface of host metabolism and the immune system.Nat ure Immunol ogy,14(7):676-684.
Caporaso J G,Bittinger K,Bushman F D,DeSantis T Z,Andersen G L,Knight R.2010b.PyNAST:a fl exible 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,Pe?a 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.Nat ure 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.T he ISMEJ ournal,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&Shellfi sh Immun ology,28(1):56-64.
De Schryver P,Vadstein O.2014.Ecological theory as a foundation to control pathogenic invasion in aquaculture.The ISME J ournal,8:2 360-2 368.
Dicksved J,Halfvarson J,Rosenquist M,J?rnerot 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 J ournal,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.Int ernational J ournal of Syst ematic Bacteriol ogy,26:459-466.
Kau A L,Ahern P P,Griffi n 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.Mol ecular Immunol ogy,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 confi rmed by polymerase chain reaction and16S rDNA sequencing.Dis eases of Aquat ic Org anisms,61(1-2):169-174.
Liu Q,Li H Y,Wang Q,Liu P,Dai F Y,Li J.2007.Identifi cation and phylogenetic analysis of a strain of Vibrio alginolyticus,a pathogen in Portunus trituberculatus with toothpaste disease.Mar ine Freshwater Res earch,28(4):9-13.(in Chinese with English abstract)
Mago?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 microfl ora 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%fi sh 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,DoréJ,Guarner F,Kristiansen K,Pedersen O,Parkhill J,Weissenbach J,MetaHIT Consortium,Bork P,Ehrlich SD,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 WC,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 defi cits and neuroinfl ammation 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-17to repair intestinal epithelial damage.Immunity,43(3):488-501.
Tremaroli,V,B?ckhed,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,Aff ourtit 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.Aquacult ure Int ernational,19(2):351-359.
Wang G X,Huang Z R,Yuan M.2007.Isolation and identifi cation of the pathogen of milk disease cultured in swimming crab Portunus tritubercula r us(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 fl ora 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&Shellfi sh Immunology,41:156-162.
Wu T,Zhang Z L,Cai C F,Ye Y T,Zhu J M,Li T.2015.The eff ect of pectin and xylan on intestinal microfl ora 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 identifi cation of Vibrio parahaemolyticus from diseased Portunus trituberculatus L.Mar ine Sci ence Bull etin,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.Identifi cation of a novel class B scavenger receptor homologue in Portunus trituberculatus:molecular cloning and microbial ligand binding.Fish&Shellfi sh Immun ology,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 specifi cally active against marine Gram-negative bacteria,produced by a marine bacterium.The J ournal of Antibiot ics,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 EC.2016.Symbiotic bacteria in gills and guts of Chinese mitten crab(Eriocheir sinensis)diff er 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.Aquacult ure Int ernational,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 E cology,72(4):975-985.
Brestoff J R,Artis D.2013.Commensal bacteria at the interface of host metabolism and the immune system.Nat ure Immunol ogy,14(7):676-684.
Caporaso J G,Bittinger K,Bushman F D,DeSantis T Z,Andersen G L,Knight R.2010b.PyNAST:a fl exible 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,Pe?a 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.Nat ure 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.T he ISMEJ ournal,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&Shellfi sh Immun ology,28(1):56-64.
De Schryver P,Vadstein O.2014.Ecological theory as a foundation to control pathogenic invasion in aquaculture.The ISME J ournal,8:2 360-2 368.
Dicksved J,Halfvarson J,Rosenquist M,J?rnerot 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 J ournal,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.Int ernational J ournal of Syst ematic Bacteriol ogy,26:459-466.
Kau A L,Ahern P P,Griffi n 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.Mol ecular Immunol ogy,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 confi rmed by polymerase chain reaction and16S rDNA sequencing.Dis eases of Aquat ic Org anisms,61(1-2):169-174.
Liu Q,Li H Y,Wang Q,Liu P,Dai F Y,Li J.2007.Identifi cation and phylogenetic analysis of a strain of Vibrio alginolyticus,a pathogen in Portunus trituberculatus with toothpaste disease.Mar ine Freshwater Res earch,28(4):9-13.(in Chinese with English abstract)
Mago?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 microfl ora 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%fi sh 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,DoréJ,Guarner F,Kristiansen K,Pedersen O,Parkhill J,Weissenbach J,MetaHIT Consortium,Bork P,Ehrlich SD,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 WC,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 defi cits and neuroinfl ammation 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-17to repair intestinal epithelial damage.Immunity,43(3):488-501.
Tremaroli,V,B?ckhed,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,Aff ourtit 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.Aquacult ure Int ernational,19(2):351-359.
Wang G X,Huang Z R,Yuan M.2007.Isolation and identifi cation of the pathogen of milk disease cultured in swimming crab Portunus tritubercula r us(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 fl ora 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&Shellfi sh Immunology,41:156-162.
Wu T,Zhang Z L,Cai C F,Ye Y T,Zhu J M,Li T.2015.The eff ect of pectin and xylan on intestinal microfl ora 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 identifi cation of Vibrio parahaemolyticus from diseased Portunus trituberculatus L.Mar ine Sci ence Bull etin,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.Identifi cation of a novel class B scavenger receptor homologue in Portunus trituberculatus:molecular cloning and microbial ligand binding.Fish&Shellfi sh Immun ology,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 specifi cally active against marine Gram-negative bacteria,produced by a marine bacterium.The J ournal of Antibiot ics,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 EC.2016.Symbiotic bacteria in gills and guts of Chinese mitten crab(Eriocheir sinensis)diff er 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.Aquacult ure Int ernational,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 E cology,72(4):975-985.