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Changes in Bacterial Communities of Kumamoto Oyster Larvae During Their Early Development and Following Vibrio Infection Resulting in a Mass Mortality Event

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Abstract

Vibrio and Ostreid herpesvirus 1 are responsible for mass mortalities of oyster larvae in hatcheries. Relevant works have focused on their relationships with the disease when larval mortality occurs. On the contrary, little is known about how the resident microbiota in oyster larvae responds to Vibrio-infected disease causing mortality as the disease progressed, whereas this knowledge is fundamental to unveil the etiology of the disease. Here, we analyzed the temporal succession of the microbiome of Kumamoto oyster (Crassostrea sikamea) larvae during their early development, accompanied by a Vibrio-caused mortality event that occurred at the post D-stage of larval development in a shellfish hatchery in Ningbo, China, on June 2020. The main causative agent of larval mortality was attributable to Vibrio infection, which was confirmed by linearly increased Vibrio abundance over disease progression. Larval bacterial communities dramatically changed over host development and disease progression, as highlighted by reduced α-diversity and less diverse core taxa when the disease occurred. Null model and phylogenetic-based mean nearest taxon distance analyses showed that the relative importance of deterministic processes governing larval bacterial assembly initially increased over host development, whereas this dominance was depleted over disease progression. Furthermore, we screened the disease-discriminatory taxa with a significant change in their relative abundances, which could be indicative of disease progression. In addition, network analysis revealed that disease occurrence remodeled the co-occurrence patterns and niche characteristics of larval microbiota. Our findings demonstrate that the dysbiosis of resident bacterial communities and the shift of microecological mechanisms in the larval microbiome may contribute to mortality during oyster early development.

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References

  • Alfaro AC, Nguyen TV, Merien F (2019) The complex interactions of Ostreid herpesvirus 1, Vibrio bacteria, environment and host factors in mass mortality outbreaks of Crassostrea gigas. Rev Aquacult 11:1148–1168

    Article  Google Scholar 

  • Arfken A, Song B, Allen SK Jr, Carnegie RB (2021) Comparing larval microbiomes of the eastern oyster (Crassostrea virginica) raised in different hatcheries. Aquaculture 531:735955

    Article  CAS  Google Scholar 

  • Bakke I, Coward E, Andersen T, Vadstein O (2015) Selection in the host structures the microbiota associated with developing cod larvae (Gadus morhua). Environ Microbiol 17:3914–3924

    Article  PubMed  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Proc 3rd Intl ICWSM Conf 3:361–362

  • Boutin S, Bernatchez L, Audet C, Derôme N (2013) Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS ONE 8:e84772

    Article  PubMed  PubMed Central  Google Scholar 

  • Bureau of Fisheries (2020) China Fisheries Statistic Yearbook 2019. China Agriculture Press, Beijing

    Google Scholar 

  • Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:1–11

    Article  Google Scholar 

  • Churchill GA (2004) Using ANOVA to analyze microarray data. Biotechniques 37:173–175

    Article  CAS  PubMed  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18:117–143

    Article  Google Scholar 

  • Clerissi C, de Lorgeril J, Petton B, Lucasson A, Escoubas JM, Gueguen Y, Dégremont L, Mitta G, Toulza E (2020) Microbiota composition and evenness predict survival rate of oysters confronted to Pacific oyster mortality syndrome. Front Microbiol 11:311

    Article  PubMed  PubMed Central  Google Scholar 

  • Csárdi G, Nepusz T (2006) The igraph software package for complex network research. InterJ Complex Syst 1695:1695

    Google Scholar 

  • Dai W, Yu W, Xuan L, Tao Z, Xiong J (2018) Integrating molecular and ecological approaches to identify potential polymicrobial pathogens over a shrimp disease progression. Appl Microbiol Biotechnol 102:3755–3764

    Article  CAS  PubMed  Google Scholar 

  • Dai W, Qiu Q, Chen J, Xiong J (2019) Gut eukaryotic disease-discriminatory taxa are indicative of Pacific white shrimp (Litopenaeus vannamei) white feces syndrome. Aquaculture 506:154–160

    Article  Google Scholar 

  • Dai W, Sheng Z, Chen J, Xiong J (2020) Shrimp disease progression increases the gut bacterial network complexity and abundances of keystone taxa. Aquaculture 517:734802

    Article  Google Scholar 

  • Dai W, Ye J, Liu S, Chang G, Xu H, Lin Z, Xue Q (2022a) Bacterial community dynamics in Kumamoto oyster Crassostrea sikamea hatchery during larval development. Front Microbiol 13:933941

    Article  PubMed  PubMed Central  Google Scholar 

  • Dai W, Ye J, Liu S, Xu H, Liu M, Lin Z, Xue Q (2022b) Prokaryotic and eukaryotic microbial community in Kumamoto oyster (Crassostrea sikamea) larvae: response to antibiotics in trace concentration. Fishes 7:272

    Article  Google Scholar 

  • de Lorgeril J, Lucasson A, Petton B, Toulza E, Montagnani C, Clerissi C, Vidal-Dupiol J, Chaparro C, Galinier R, Escoubas JM, Haffner P, Dégremont L, Charrière GM, Lafont M, Delort A, Vergnes A, Chiarello M, Faury N, Rubio T, Leroy MA, Pérignon A, Régler D, Morga B, Alunno-Bruscia M, Boudry P, Le Roux F, Destoumieux-Garzόn D, Gueguen Y, Mitta G (2018) Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nat Commun 9:4215

    Article  PubMed  PubMed Central  Google Scholar 

  • De Schryver P, Vadstein O (2014) Ecological theory as a foundation to control pathogenic invasion in aquaculture. ISME J 8:2360–2368

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Erdos P, Rényi A (1960) On the evolution of random graphs. Publ Math Inst Hung Acad Sci 5:17–60

    Google Scholar 

  • Fallet M, Montagnani C, Petton B, Dantan L, de Lorgeril J, Comarmond S, Chaparro C, Toulza E, Boitard S, Escoubas JM, Vergnes A, Le Grand J, Bulla I, Gueguen Y, Vidal-Dupiol J, Grunau C, Mitta G, Cosseau C (2022) Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection. Microbiome 10:85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallego S, Vila J, Nieto JM, Urdiain M, Rosselló-Móra R, Grifoll M (2010) Breoghania corrubedonensis gen. nov. sp. nov., a novel alphaproteobacterium isolated from a Galician beach (NW Spain) after the Prestige fuel oil spill, and emended description of the family Cohaesibacteraceae and the species Cohaesibacter gelatinilyticus. Syst Appl Microbiol 33:316–321

  • Genard B, Pernet F, Lemarchand K, Boudry P, Moraga D, Tremblay R (2011) Physiological and biochemical changes associated with massive mortality events occurring in larvae of American oyster (Crassostrea virginica). Aquat Living Resour 24:247–260

    Article  CAS  Google Scholar 

  • Green TJ, Siboni N, King WL, Labbate M, Seymour JR, Raftos D (2019) Simulated marine heat wave alters abundance and structure of Vibrio populations associated with the Pacific Oyster resulting in a mass mortality event. Microb Ecol 77:736–747

    Article  PubMed  Google Scholar 

  • Groussin M, Mazel F, Alm EJ (2020) Co-evolution and co-speciation of host-gut Bacteria systems. Cell Host Microbe 28:12–22

    Article  CAS  PubMed  Google Scholar 

  • Hamilton N (2015) An extension to ‘ggplot2’, for the creation of ternary diagrams. Anesthesiology 64:72–86

    Google Scholar 

  • Harris JM (1993) The presence nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25:195–231

    Article  CAS  PubMed  Google Scholar 

  • Holt CC, Bass D, Stentiford GD, van der Giezen M (2021) Understanding the role of the shrimp gut microbiome in health and disease. J Invertebr Pathol 186:107387

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Li X, Wang L, Shao Z (2016) Changes in the intestinal bacterial community during the growth of white shrimp. Litopenaeus Vannamei Aquac Res 47:1737–1746

    Article  Google Scholar 

  • Huang Z, Zeng S, Xiong J, Hou D, Zhou R, Xing C, Wei D, Deng X, Yu L, Wang H, Deng Z, Weng S, Kriengkrai S, Ning D, Zhou J, He J (2020) Microecological Koch’s postulates reveal that intestinal microbiota dysbiosis contributes to shrimp white feces syndrome. Microbiome 8:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins C, Hick P, Gabor M, Spiers Z, Fell SA, Gu X, Read A, Go J, Dove M, O’Connor W, Kirkland PD, Frances J (2013) Identification and characterisation of an ostreid herpesvirus-1 microvariant (OsHV-1 micro-var) in Crassostrea gigas (Pacific oysters) in Australia. Dis Aquat Org 105:109–126

    Article  CAS  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kesarcodi-Watson A, Miner P, Nicolas JL, Robert R (2012) Protective effect of four potential probiotics against pathogen-challenge of the larvae of three bivalves: Pacific oyster (Crassostrea gigas), flat oyster (Ostrea edulis) and scallop (Pecten maximus). Aquaculture 344:29–34

    Article  Google Scholar 

  • Kim HJ, Jun JW, Giri SS, Chi C, Yun S, Kim SG, Kim SW, Han SJ, Kwon J, Oh WT, Lee SB, Kim JH, Park SC (2020) Identification and genome analysis of Vibrio coralliilyticus causing mortality of Pacific oyster (Crassostrea gigas) larvae. Pathogens 9:206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lan Y, Wang Q, Cole JR, Rosen GL (2012) Using the RDP classifier to predict taxonomic novelty and reduce the search space for finding novel organisms. PLoS ONE 7:e32491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lasa A, di Cesare A, Tassistro G, Borello A, Gualdi S, Furones D, Carrasco N, Cheslett D, Brechon A, Paillard C, Bidault A, Pernet F, Canesi L, Edomi P, Pallavicini A, Pruzzo C, Vezzulli L (2019) Dynamics of the Pacific oyster pathobiota during mortality episodes in Europe assessed by 16S rRNA gene profiling and a new target enrichment next-generation sequencing strategy. Environ Microbiol 21:4548–4562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YF, Chen YW, Xu JK, Ding WY, Shao AQ, Zhu YT, Wang C, Liang X, Yang JL (2019) Temperature elevation and Vibrio cyclitrophicus infection reduce the diversity of haemolymph microbiome of the mussel Mytilus coruscus. Sci Rep 9:16391

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Z, Nicolae VV, Akileh R, Liu T (2017) A brief review of oyster-associated microbiota. Microbiol Res J Int 20:14

    Article  Google Scholar 

  • Luna-Gonzalez A, Maeda-Martínez A, Sainz J, Ascencio-Valle F (2002) Comparative susceptibility of veliger larvae of four bivalve mollusks to a Vibrio alginolyticus strain. Dis Aquat Organ 49:221–226

    Article  CAS  PubMed  Google Scholar 

  • Mallon CA, Elsas JD, Salles JF (2015) Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol 23:719–729

    Article  CAS  PubMed  Google Scholar 

  • Modak TH, Gomez-Chiarri M (2020) Contrasting immunomodulatory effects of probiotic and pathogenic bacteria on Eastern oyster, Crassostrea virginica, larvae. Vaccines 8:588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolas JL, Corre S, Cochard JC (2004) Bacterial population association with phytoplankton cultured in a bivalve hatchery. Microb Ecol 48:400–413

    Article  PubMed  Google Scholar 

  • Paillard C, Gueguen Y, Wegner KM, Bass D, Pallavicini A, Vezzulli L, Arzul I (2022) Recent advances in bivalve-microbiota interactions for disease prevention in aquaculture. Curr Opin Biotech 73:225–232

    Article  CAS  PubMed  Google Scholar 

  • Petton B, Pernet F, Robert R, Boudry P (2013) Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquac Environ Interact 3:257–273

    Article  Google Scholar 

  • Prado S, Romalde JL, Montes J, Barja JL (2005) Pathogenic bacteria isolated from disease outbreaks in shellfish hatcheries. First description of Vibrio neptunius as an oyster pathogen. Dis Aquat Organ 67:209–215

  • Prado S, Romalde JL, Barja JL (2010) Review of probiotics for use in bivalve hatcheries. Vet Microbiol 145:187–197

    Article  PubMed  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490

    Article  PubMed  PubMed Central  Google Scholar 

  • Pruzzo C, Gallo G, Canesi L (2005) Persistence of Vibrios in marine bivalves: the role of interactions with haemolymph components. Environ Microbiol 7:761–772

    Article  PubMed  Google Scholar 

  • Qu L, Lai Q, Zhu F, Hong X, Sun X, Shao Z (2011) Cohaesibacter marisflavi sp. nov., isolated from sediment of a seawater pond used for sea cucumber culture, and emended description of the genus Cohaesibacter. Int J Syst Evol Microbiol 61:762–766

  • R Development Core Team (2013) R: a language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria ISBN: 3–900051–07–0. Available online at: https://www.R-project.org/

  • Renault T, Bouquet AL, Maurice JT, Lupo C, Blachier P (2014) Ostreid herpesvirus 1 infection among Pacific oyster (Crassostrea gigas) spat: relevance of water temperature to virus replication and circulation prior to the onset of mortality. Appl Environ Microbiol 80:5419–5426

    Article  PubMed  PubMed Central  Google Scholar 

  • Richards GP, Watson MA, Needleman DS, Church KM, Häse CC (2015) Mortalities of Eastern and Pacific oyster larvae caused by the pathogens Vibrio coralliilyticus and Vibrio tubiashii. Appl Environ Microb 81:292–297

    Article  Google Scholar 

  • Rodríguez-Ramos T, Carpio Y, Bolívar J, Gómez L, Estrada MP, Pendón C (2016) Nitric oxide synthase-dependent immune response against gram negative bacteria in a crustacean, Litopenaeus vannamei. Fish Shellfish Immunol 50:50–55

    Article  PubMed  Google Scholar 

  • Rojas R, Miranda CD, Opazo R, Romero J (2015) Characterization and pathogenicity of Vibrio splendidus strains associated with massive mortalities of commercial hatchery-reared larvae of scallop Argopecten purpuratus (Lamarck, 1819). J Invertebr Pathol 124:61–69

    Article  PubMed  Google Scholar 

  • Savin-Amador M, Rojas-Contreras M, Arce-Amézquita PM, Rangel-Dávalos C, Vázquez-Juárez R (2021) Lactobacillus strains isolated from oysters improve the production of Crassostrea gigas larvae. Lat Am J Aquat Res 49:551–564

    Article  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    Article  PubMed  PubMed Central  Google Scholar 

  • Simons AL, Churches N, Nuzhdin S (2018) High turnover of faecal microbiome from algal feedstock experimental manipulations in the Pacific oyster (Crassostrea gigas). Microb Biotechnol 11:848–858

    Article  PubMed  PubMed Central  Google Scholar 

  • Solomieu VB, Renault T, Travers MA (2015) Mass mortality in bivalves and the intricate case of the Pacific oyster, Crassostrea gigas. J Invertebr Pathol 131:2–10

    Article  Google Scholar 

  • Srivastava DS, Cadotte MW, Macdonald A, Marushia RG, Mirotchnick N (2012) Phylogenetic diversity and the functioning of ecosystems. Ecol Lett 15:637–648

    Article  PubMed  Google Scholar 

  • Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rochhold M, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Stegen JC, Lin X, Fredrickson JK, Konopka AE (2015) Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol 6:370

    Article  PubMed  PubMed Central  Google Scholar 

  • Stephens WZ, Burns AR, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM (2016) The composition of the zebrafish intestinal microbial community varies across development. ISME J 10:644–654

    Article  PubMed  Google Scholar 

  • Stevick RJ, Sohn S, Modak TH, Nelson DR, Rowley DC, Tammi K, Smolowitz R, Lundgren KM, Post AF, Gomez-Chiarri M (2019) Bacterial community dynamics in an oyster hatchery in response to probiotic treatment. Front Microbiol 10:1060

    Article  PubMed  PubMed Central  Google Scholar 

  • Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. P Natl A Sci 108:17480–17485

    Article  CAS  Google Scholar 

  • Thompson JR, Randa MA, Marcelino LA, Tomita-Mitchell A, Lim E, Polz MF (2004) Diversity and dynamics of a North Atlantic coastal Vibrio community. Appl Environ Microbiol 70:4103–4110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trabal Fernández N, Mazón-Suástegui JM, 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 Microbiol Ecol 88:69–83

    Article  PubMed  Google Scholar 

  • Trabal N, Mazón-Suástegui JM, Vázquez-Juárez R, Asencio-Valle F, Morales-Bojórquez E, Romero J (2012) Molecular analysis of bacterial microbiota associated with oysters (Crassostrea gigas and Crassostrea corteziensis) in different growth phases at two cultivation sites. Microb Ecol 64:555–569

    Article  CAS  PubMed  Google Scholar 

  • Travers MA, Miller KB, Roque A, Friedman CS (2015) Bacterial diseases in marine bivalves. J Invertebr Pathol 131:11–31

    Article  PubMed  Google Scholar 

  • Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206

    Article  PubMed  Google Scholar 

  • Vonaesch P, Anderson M, Sansonetti PJ (2018) Pathogens, microbiome and the host: emergence of the ecological Koch’s postulates. FEMS Microbiol Rev 42:273–292

    Article  CAS  PubMed  Google Scholar 

  • Wallace RK, Waters P, Rikard FS (2008) Oyster hatchery techniques. Southern Regional Aquaculture Center No. 4302

  • Wang Y, Wang K, Huang L, Dong P, Wang S, Chen H, Lu Z, Hou D, Zhang D (2020) Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle. Microbiome 8:106

    Article  PubMed  PubMed Central  Google Scholar 

  • Webb CO, Ackerly DD, Mcpeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Webb SC, Fidler A, Renault T (2007) Primers for PCR-based detection of ostreid herpes virus-1 (OsHV-1): application in a survey of New Zealand mollusks. Aquaculture 272:126–139

    Article  CAS  Google Scholar 

  • Wei Y, Ren T, Zhang L (2020) Dix-seq: an integrated pipeline for fast amplicon data analysis. BioRxiv. https://doi.org/10.1101/2020.05.11.089748

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao F, Zhu W, Yu Y, He Z, Yan Q (2021) Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota. npj Biofilms Microbiomes 7:5

  • Xiong J, Zhu J, Zhang D (2014) The application of bacterial indicator phylotypes to predict shrimp health status. Appl Microbiol Biotechnol 98:8291–8299

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Zhu J, Dai W, Dong C, Qiu Q, Li C (2017) Integrating gut microbiota immaturity and disease-discriminatory taxa to diagnose the initiation and severity of shrimp disease. Environ Microbiol 19:1490–1501

    Article  PubMed  Google Scholar 

  • Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, Kempher ML, Wu L, Wang Y, Liao L, Li X, Wu S, Ni J, Wang C, Zhou J (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 18:4739–4754

    Article  CAS  PubMed  Google Scholar 

  • Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Li D, Refaey MM, Xu W, Tang R, Li L (2018) Host age affects the development of southern catfish gut bacterial community divergent from that in the food and rearing water. Front MIcrobiol 9:495

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was financially supported by the National Natural Science Foundation of China (32202989), “3315” Innovative Team Project of Ningbo City, Zhejiang Province Natural Science Foundation (LQ22C190005), Key Research and Development Program of Zhejiang Province (2019C02054), China Agriculture Research System of MOF and MARA, and Research Plan Project of Zhejiang Wanli University.

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  1. Ninghai Institute of Mariculture Breeding and Seed Industry, Zhejiang Wanli University, Ningbo, China

    Wenfang Dai, Qinggang Xue, Sheng Liu, Hongqiang Xu, Minhai Liu & Zhihua Lin

  2. Zhejiang Key Laboratory of Aquatic Germplasm Resource, College of Biological and Environmental Sciences, Zhejiang Wanli University, Ningbo, China

    Wenfang Dai, Jing Ye, Qinggang Xue, Sheng Liu, Hongqiang Xu, Minhai Liu & Zhihua Lin

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  1. Wenfang Dai
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QX and ZL conceived and designed the study. JY performed the experiments. SL, ML, and HX collected the samples. WD analyzed the data and wrote and revised the manuscript. All authors read and approved the manuscript.

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Dai, W., Ye, J., Xue, Q. et al. Changes in Bacterial Communities of Kumamoto Oyster Larvae During Their Early Development and Following Vibrio Infection Resulting in a Mass Mortality Event. Mar Biotechnol 25, 30–44 (2023). https://doi.org/10.1007/s10126-022-10178-0

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