Cite this paper:
Hongxia WANG, Xin YUE, Jiajia YU, Rui WANG, Shuangshuang TENG, Jun FANG, Baozhong LIU. Microbial community changes in the digestive tract of the clam Meretrix petechialis in response to Vibrio parahaemolyticus challenge[J]. Journal of Oceanology and Limnology, 2021, 39(1): 329-339

Microbial community changes in the digestive tract of the clam Meretrix petechialis in response to Vibrio parahaemolyticus challenge

Hongxia WANG1,2, Xin YUE1,2, Jiajia YU1, Rui WANG1, Shuangshuang TENG3,4, Jun FANG3,4, Baozhong LIU1,2
1 CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, China;
3 Zhejiang Mariculture Research Institute, Wenzhou 325005, China;
4 Zhejiang Key Laboratory of Exploitation and Preservation of Coastal Bio-resource, Wenzhou 325005, China
Abstract:
Disease in clams frequently occurred over the last decade and has become a serious threat to the clam aquaculture industry and natural stocks. Mass clam mortality events were reported to be associated with the presence of opportunistic pathogen vibrio. However, the complexity of infection that occurs in the natural environment remains poorly understood. In this study, we smulated a natural disease outbreak by vibrio immersion infection to study the diversity and dynamics of microbiota in the digestive tract of clam Meretrix petechialis during the infection process. Dramatic changes in operational taxonomic unit richness and phylum composition of the bacterial communities were observed during pathogen invasion. In addition, we investigated the potential relationship between microbiota dynamics and host status during disease progression. Results reveal that, at the end stage of vibrio infection, interindividual variation in the digestive tract microbiota increased, as did the difference in individual health status. The moribund clams displayed signs of microbial community shifts to low diversity, and the microbial community was characterized by mass proliferation of a few operational taxonomic units.
Key words:    Meretrix petechialis|vibrio challenge|16S ribosomal RNA|bacterial community|digestive tract   
Received: 2019-08-29   Revised: 2020-01-15
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Articles by Hongxia WANG
Articles by Xin YUE
Articles by Jiajia YU
Articles by Rui WANG
Articles by Shuangshuang TENG
Articles by Jun FANG
Articles by Baozhong LIU
References:
Allam B, Espinosa E P. 2016. Bivalve immunity and response to infections:are we looking at the right place? Fish & Shellfish Immunology, 53:4-12.
Bernal M G, Fernández N T, Lastra P E S, Marrero R M, Mazón-Suástegui J M. 2017. Streptomyces effect on the bacterial microbiota associated to Crassostrea sikamea oyster. Journal of Applied Microbiology, 122(3):601-614.
Boutin S, Bernatchez L, Audet C, Derôme D. 2013. Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS One, 8(12):e84772.
Campbell B J, Yu L Y, Heidelberg J F, Kirchman D L. 2011.Activity of abundant and rare bacteria in a coastal ocean.Proceedings of the National Academy of Sciences of the United States of America, 108(31):12 776-12 781.
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. 2010. QⅡME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5):335-336.
Chang J Y, Antonopoulos D A, Kalra A, Tonelli A, Khalife W, Schmidt T, Young V B. 2008. Decreased diversity of the fecal microbiome in recurrent Clostridium difficileassociated diarrhea. Journal of Infectious Diseases, 197(3):435-438.
Chen W Y, Ng T H, Wu J H, Chen J W, Wang H C. 2017.Microbiome dynamics in a shrimp grow-out pond with possible outbreak of acute hepatopancreatic necrosis disease. Scientific Reports, 7:9395.
de Lorgeril J, Lucasson A, Petton B, Toulza E, Montagnani C, Clerissi C, Vidal-Dupiol J, Chaparro C, Galinier R, Escoubas J M, Haffner P, Dégremont L, Charrière G M, Lafont M, Delort A, Vergnes A, Chiarello M, Faury N, Rubio T, Leroy M A, Pérignon A, Régler D, Morga B, Alunno-Bruscia M, Boudry P, Le Roux F, DestoumieuxGarzón D, Gueguen Y, Mitta G. 2018. Immunesuppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nature Communications, 9:4 215, https://doi.org/10.1038/s41467-018-06659-3.
Dupuy C, Vaquer A, Lam-Höai T, Rougier C, Mazouni N, Lautier J, Collos Y, Le Gall S. 2000. Feeding rate of the oyster Crassostrea gigas in a natural planktonic community of the Mediterranean Thau Lagoon. Marine Ecology Progress Series, 205:171-184.
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. 2013. UPARSE:highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10):996-998.
Espinosa E P, Koller A, Allam B. 2016. Proteomic characterization of mucosal secretions in the eastern oyster, Crassostrea virginica. Journal of Proteomics, 132:63-76.
Fan L, Liu M, Simister R, Webster N S, Thomas T. 2013.Marine microbial symbiosis heats up:the phylogenetic and functional response of a sponge holobiont to thermal stress. The ISME Journal, 7(5):991-1 002.
Fernández N T, Mazón-Suástegui J M, Vázquez-Juárez R, Ascencio-Valle F, Romero J. 2014. Changes in the composition and diversity of the bacterial microbiota associated with oysters (Crassostrea corteziensis, Crassostrea gigas and Crassostrea sikamea) during commercial production. FEMS Microbiology Ecology, 88(1):69-83.
Garnier M, Labreuche Y, Garcia C, Robert M, Nicolas J L. 2007. Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microbial Ecology, 53(2):187-196.
Gobet A, Böer S I, Huse S M, van Beusekom J E E, Quince C, Sogin M L, Boetius A, Ramette A. 2012. Diversity and dynamics of rare and of resident bacterial populations in coastal sands. The ISME Journal, 6(3):542-553.
Green T J, Barnes A C. 2010. Bacterial diversity of the digestive gland of Sydney rock oysters, Saccostrea glomerata infected with the paramyxean parasite, Marteilia sydneyi. Journal of Applied Microbiology, 109(2):613-622.
Ha E M, Oh C T, Bae Y S, Lee W J. 2005. A direct role for dual oxidase in Drosophila gut immunity. Science, 310(5749):847-850.
Hamady M, Lozupone C, Knight R. 2010. Fast UniFrac:facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. The ISME Journal, 4(1):17-27.
King G M, Judd C, Kuske C R, Smith C. 2012. Analysis of stomach and gut microbiomes of the eastern oyster(Crassostrea virginica) from coastal Louisiana, USA.PLoS One, 7(12):e51475.
Li H Y, Wang H, Wang H T, Xin P Y, Xu X H, Ma Y, Liu W P, Teng C Y, Jiang C L, Lou L P, Arnold W, Cralle L, Zhu Y G, Chu J F, Gilbert J A, Zhang Z J. 2018. The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales.Microbiome, 6:187.
Liang B B, Jiang F J, Zhang S J, Yue X, Wang H X, Liu B Z. 2017. Genetic variation in vibrio resistance in the clam Meretrix petechialis under the challenge of Vibrio parahaemolyticus. Aquaculture, 468:458-463.
Lokmer A, Kuenzel S, Baines J F, Wegner K M. 2016. The role of tissue-specific microbiota in initial establishment success of Pacific oysters. Environmental Microbiology, 18(3):970-987.
Lokmer A, Wegner K M. 2015. Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. The ISME Journal, 9(3):670-682.
Olson J B, Thacker R W, Gochfeld D J. 2014. Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the Caribbean sponge Aplysina cauliformis. FEMS Microbiology Ecology, 87(1):268-279.
Petton B, Bruto M, James A, Labreuche Y, Alunno-Bruscia M, Le Roux F. 2015. Crassostrea gigas mortality in France:the usual suspect, a herpes virus, may not be the killer in this polymicrobial opportunistic disease. Frontiers in Microbiology, 6:686.
Preheim S P, Boucher Y, Wildschutte H, David L A, Veneziano D, Alm E J, Polz M F. 2011. Metapopulation structure of Vibrionaceae among coastal marine invertebrates.Environmental Microbiology, 13(1):265-275.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner F O. 2013. The SILVA ribosomal RNA gene database project:improved data processing and web-based tools. Nucleic Acids Research, 41(D1):D590-D596.
Råberg L, Sim D, Read A F. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318(5851):812-814.
Rőszer T. 2014. The invertebrate midintestinal gland("hepatopancreas") is an evolutionary forerunner in the integration of immunity and metabolism. Cell and Tissue Research, 358(3):685-695.
Schmitt P, Rosa R D, Duperthuy M, de Lorgeril J, Bachère E, Destoumieux-Garzón D. 2012. The antimicrobial defense of the Pacific oyster, Crassostrea gigas. How diversity may compensate for scarcity in the regulation of resident/pathogenic microflora. Frontiers in Microbiology, 3:160.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W S, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology, 12:R60.
Tanaka R, Ootsubo M, Sawabe T, Ezura Y, Tajima K. 2004.Biodiversity and in situ abundance of gut microflora of abalone (Haliotis discus hannai) determined by cultureindependent techniques. Aquaculture, 241(1-4):453-463.
Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16):5 261-5 267.
Wegner K M, Volkenborn N, Peter H, Eiler A. 2013.Disturbance induced decoupling between host genetics and composition of the associated microbiome. BMC Microbiology, 13:252.
Wendling C C, Batista F M, Wegner K M. 2014. Persistence, seasonal dynamics and pathogenic potential of vibrio communities from Pacific oyster hemolymph. PLoS One, 9(4):e94256.
Xiong J B, Wang K, Wu J F, Qiuqian L 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, Yu W N, Dai W F, Zhang J J, Qiu Q F, Ou C R. 2018. Quantitative prediction of shrimp disease incidence via the profiles of gut eukaryotic microbiota. Applied Microbiology and Biotechnology, 102(7):3 315-3 326.
Xiong J B. 2018. Progress in the gut microbiota in exploring shrimp disease pathogenesis and incidence. Applied Microbiology and Biotechnology, 102(17):7 343-7 350.
Yang H T, Yang M C, Sun J J, Shi X Z, Zhao X F, Wang J X. 2016. Dual oxidases participate in the regulation of intestinal microbiotic homeostasis in the kuruma shrimp Marsupenaeus japonicus. Developmental & Comparative Immunology, 59:153-163.
Yang H T, Zou S S, Zhai L J, Wang Y, Zhang F M, An L G, Yang G W. 2017. Pathogen invasion changes the intestinal microbiota composition and induces innate immune responses in the zebrafish intestine. Fish & Shellfish Immunology, 71:35-42.
Yu J J, Wang H X, Yue X, Liu B Z. 2019a. Dynamic immune and metabolism response of clam Meretrix petechialis to Vibrio challenge revealed by a time series of transcriptome analysis. Fish & Shellfish Immunology, 94:17-26.
Yu Z C, Liu C, Fu Q, Lu G X, Han S, Wang L L, Song L S. 2019b. The differences of bacterial communities in the tissues between healthy and diseased Yesso scallop(Patinopecten yessoensis). AMB Express, 9:148.
Yue X, Liu B Z, Xiang J H, Jia J T. 2010. Identification and characterization of the pathogenic effect of a Vibrio parahaemolyticus-related bacterium isolated from clam Meretrix meretrix with mass mortality. Journal of Invertebrate Pathology, 103(2):109-115.
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