Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster <italic style="font-style: italic">Crassostrea gigas</italic>

Qiang FU; Zichao YU; Junyan ZHAO; Lei GAO; Ning KONG; Lingling WANG; Linsheng SONG

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Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas

Aquaculture and Fisheries | Updated：2024-10-11

- Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas
- Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas
- 海洋湖沼学报(英文) 2024年42卷第4期页码：1348-1358
- Affiliations：
  
  1.Liaoning Key Laboratory of Marine Animal Immunology and Disease Control, Dalian Ocean University, Dalian 116023, China
  2.Functional Laboratory of Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
  3.Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai 519000, China
  4.Dalian Key Laboratory of Aquatic Animal Disease Prevention and Control, Dalian Ocean University, Dalian 116023, China
- Author bio：
  
  kongning@dlou.edu.cn;
  wanglingling@dlou.edu.cn
- Funds：
  
  the National Natural Science Foundation of China(41961124009);the Earmarked Fund for China Agriculture Research System(CARS-49);the fund for Outstanding Talents and Innovative Team of Agricultural Scientific Research from MARA, the Innovation Team of Aquaculture Environment Safety from Liaoning Province(LT202009);the Dalian High Level Talent Innovation Support Program(2022RG14)
- DOI：
  中图分类号：
- 收稿：2023-09-18，
  
  网络首发：2023-12-15，
  
  纸质出版：2024-07-01
- Accepted：
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Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas[J]. 海洋湖沼学报(英文), 2024,42(4):1348-1358.

FU Qiang,YU Zichao,ZHAO Junyan,et al.Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster ,Crassostrea gigas[J].Journal of Oceanology and Limnology,2024,42(04):1348-1358.
Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas[J]. 海洋湖沼学报(英文), 2024,42(4):1348-1358. DOI：

FU Qiang,YU Zichao,ZHAO Junyan,et al.Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster ,Crassostrea gigas[J].Journal of Oceanology and Limnology,2024,42(04):1348-1358. DOI：

摘要

Abstract

The Pacific oyster

Crassostrea

gigas

one of the most exploited molluscs in the world

has suffered from massive mortality in recent decades

and the occurrence mechanisms have not been well-characterized. In this study

to reveal the relationship of associated microbiota to the fitness of oysters

temporal dynamics of microbiota in the gill

hemolymph

and hepatopancreas of

gigas

during April 2018‍–‍January 2‍019 were investigated by

16S rRNA gene sequencing. The microbiota in

gigas

exhibited tissue heterogeneity

of which Spirochaetaceae was dominant in the gill and hemolymph while Mycoplasmataceae enriched in the hepatopancreas. Co-occurrence network demonstrated that the gill microbiota exhibited higher inter-taxon connectivity while the hemolymph microbiota had more modules. The richness (Chao1 index) and diversity (Shannon index) of microbial community in each tissue showed no significant seasonal variations

except for the hepatopancreas having a higher richness in the autumn. Similarly

beta diversity analysis indicated a relatively stable microbiota in each tissue during the sampling period

showing relative abundance of the dominant taxa exhibiting temporal dynamics. Results indicate that the microbial community in

gigas

showed a tissue-specific stability with temporal dynamics in the composition

which might be essential for the tissue functioning and environmental adaption in oysters. This work provides a baseline microbiota in

gigas

and is helpful for the understanding of host-microbiota interaction in oysters.

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references

Amir A , McDonald D , Navas-Molina J A et al . 2017 . Deblur rapidly resolves single-nucleotide community sequence patterns . mSystems , 2 ( 2 ): e00191 - 16 , https://doi.org/10.1128/mSystems.00191-16 https://doi.org/10.1128/mSystems.00191-16 .

Apprill A , Weber L G , Santoro A E . 2016 . Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes . mSystems , 1 ( 5 ): e00143 - 16 , https://doi.org/10.1128/mSystems.00143-16 https://doi.org/10.1128/mSystems.00143-16 .

Banerjee S , Schlaeppi K , van der Heijden M G A . 2018 . Keystone taxa as drivers of microbiome structure and functioning . Nature Reviews Microbiology , 16 ( 9 ): 567 - 576 , https://doi.org/10.1038/s41579-018-0024-1 https://doi.org/10.1038/s41579-018-0024-1 .

Bevins C L , Salzman N H . 2011 . The potter's wheel: the host's role in sculpting its microbiota . Cellular and Molecular Life Sciences , 68 ( 22 ): 3675 - 3685 , https://doi.org/10.1007/s00018-011-0830-3 https://doi.org/10.1007/s00018-011-0830-3 .

Bolyen E , Rideout J R , Dillon M R et al . 2019 . Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 . Nature Biotechnology , 37 ( 8 ): 852 - 857 , https://doi.org/10.1038/s41587-019-0209-9 https://doi.org/10.1038/s41587-019-0209-9 .

Costello E K , Lauber C L , Hamady M et al . 2009 . Bacterial community variation in human body habitats across space and time . Science , 326 ( 5960 ): 1694 - 1697 , https://doi.org/10.1126/science.1177486 https://doi.org/10.1126/science.1177486 .

Coyte K Z , Schluter J , Foster K R . 2015 . The ecology of the microbiome: networks, competition, and stability . Science , 350 ( 6261 ): 663 - 666 , https://doi.‍org/10.1126/science.aad2602 https://doi.‍org/10.1126/science.aad2602 . https://do 10.1126/science.aad2602 http://dx.doi.org/10.1126/science.aad2602

Desriac F , El Harras A , Simon M et al . 2020 . Alterins produced by oyster-associated Pseudoalteromonas are antibacterial cyclolipopeptides with LPS-binding activity . Marine Drugs , 18 ( 12 ): 630 , https://doi.‍org/10.3390/md18120630 https://doi.‍org/10.3390/md18120630 . https://do 10.3390/md18120630 http://dx.doi.org/10.3390/md18120630

Dethlefsen L , Relman D A . 2011 . Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation . Proceedings of the National Academy of Sciences of the United States of America , 108 ( S1 ): 4554 - 4561 , https://doi.org/10.1073/pnas.1000087107 https://doi.org/10.1073/pnas.1000087107 .

Dubé C E , Ky C L , Planes S . 2019 . Microbiome of the black-lipped pearl oyster Pinctada margaritifera , a multi-tissue description with functional profiling . Frontiers in Microbiology , 10 : 1548 , https://doi.org/10.3389/fmicb.2019.01548 https://doi.org/10.3389/fmicb.2019.01548 .

Dupont S , Lokmer A , Corre E et al . 2020 . Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses . Animal Microbiome , 2 ( 1 ): 12 , https://doi.org/10.1186/s42523-020-00032-w https://doi.org/10.1186/s42523-020-00032-w .

Faith J J , Guruge J L , Charbonneau M et al . 2013 . The long-term stability of the human gut microbiota . Science , 341 ( 6141 ): 1237439 , https://doi.org/10.1126/science.1237439 https://doi.org/10.1126/science.1237439 .

Feng W W , Liu J , Cheng H et al . 2022 . Dietary compounds in modulation of gut microbiota-derived metabolites . Frontiers in Nutrition , 9 : 939571 , https://doi.org/10.3389/fnut.2022.939571 https://doi.org/10.3389/fnut.2022.939571 .

Gittenberger A , Voorbergen-Laarman M A , Engelsma M Y . 2016 . Ostreid herpesvirus OsHV-1 μVar in Pacific oysters Crassostrea gigas (Thunberg 1793) of the Wadden Sea, a UNESCO world heritage site . Journal of Fish Diseases , 39 ( 1 ): 105 - 109 , https://doi.org/10.1111/jfd.12332 https://doi.org/10.1111/jfd.12332 .

Go J , Deutscher A T , Spiers Z B et al . 2017 . Mass mortalities of unknown aetiology in Pacific oysters Crassostrea gigas in Port Stephens, New South Wales, Australia . Diseases of Aquatic Organisms , 125 ( 3 ): 227 - 242 , https://doi.org/10.3354/dao03146 https://doi.org/10.3354/dao03146 .

Green T J , Siboni N , King W L et al . 2019 . Simulated marine heat wave alters abundance and structure of Vibrio populations associated with the Pacific oyster resulting in a mass mortality event . Microbial Ecology , 77 ( 3 ): 736 - 747 , https://doi.org/10.1007/s00248-018-1242-9 https://doi.org/10.1007/s00248-018-1242-9 .

Greiner L L , Humphrey D C , Holland S N et al . 2022 . The validation of the existence of the entero-mammary pathway and the assessment of the differences of the pathway between first and third parity sows . Translational Animal Science , 6 ( 2 ): txac 047 , https://doi.org/10.1093/tas/txac047 https://doi.org/10.1093/tas/txac047 .

Hooda S , Boler B M V , Serao M C R et al . 2012 . 454 Pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber . The Journal of Nutrition , 142 ( 7 ): 1259 - 1265 , https://doi.org/10.3945/jn.112.158766 https://doi.org/10.3945/jn.112.158766 .

Horodesky A , Castilho-Westphal G G , Dal Pont G et al . 2020 . Metagenomic analysis of the bacterial microbiota associated with cultured oysters ( Crassostrea sp.) in estuarine environments . Anais da Academia Brasileira de Ciências , 92 ( S1 ): e20180432 , https://doi.‍org/10.1590/0001-3765202020180432 https://doi.‍org/10.1590/0001-3765202020180432 . https://do 10.1590/0001-3765202020180432 http://dx.doi.org/10.1590/0001-3765202020180432

King W L , Siboni N , Kahlke T et al . 2020 . Regional and oyster microenvironmental scale heterogeneity in the Pacific oyster bacterial community . FEMS Microbiology Ecology , 96 ( 5 ): fiaa 054 , https://doi.org/10.1093/femsec/fiaa054 https://doi.org/10.1093/femsec/fiaa054 .

Le Roux F , Wegner K M , Polz M F . 2016 . Oysters and vibrios as a model for disease dynamics in wild animals . Trends in Microbiology , 24 ( 7 ): 568 - 580 , https://doi.org/10.1016/j.tim.2016.03.006 https://doi.org/10.1016/j.tim.2016.03.006 .

Leadbetter J R , Schmidt T M , Graber J R et al . 1999 . Acetogenesis from H 2 plus CO 2 by spirochetes from termite guts . Science , 283 ( 5402 ): 686 - 689 , https://doi.org/10.1126/science.283.5402.686 https://doi.org/10.1126/science.283.5402.686 .

Lokmer A , Goedknegt M A , Thieltges D W et al . 2016a . Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales . Frontiers in Microbiology , 7 : 1367 , https://doi.org/10.3389/fmicb.2016.01367 https://doi.org/10.3389/fmicb.2016.01367 .

Lokmer A , Kuenzel S , Baines J F et al . 2016b . The role of tissue-specific microbiota in initial establishment success of Pacific oysters . Environmental Microbiology , 18 ( 3 ): 970 - 987 , https://doi.org/10.1111/1462-2920.13163 https://doi.org/10.1111/1462-2920.13163 .

Mansuy-Aubert V , Ravussin Y . 2023 . Short chain fatty acids: the messengers from down below . Frontiers in Neuroscience , 17 : 1197759 , https://doi.org/10.3389/fnins.2023.1197759 https://doi.org/10.3389/fnins.2023.1197759 .

Mizutani Y , Mori T , Miyazaki T et al . 2020 . Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea . PeerJ , 8 : e9326 , https://doi.org/10.7717/peerj.9326 https://doi.org/10.7717/peerj.9326 .

Nam B H , Jang J , Caetano-Anolles K et al . 2018 . Microbial community and functions associated with digestion of algal polysaccharides in the visceral tract of Haliotis discus hannai : insights from metagenome and metatranscriptome analysis . PLoS One , 13 ( 10 ): e0205594 , https://doi.org/10.1371/journal.pone.0205594 https://doi.org/10.1371/journal.pone.0205594 .

Neu A T , Hughes I V , Allen E E et al . 2021 . Decade-scale stability and change in a marine bivalve microbiome . Molecular Ecology , 30 ( 5 ): 1237 - 1250 , https://doi.‍org/10.1111/mec.15796 https://doi.‍org/10.1111/mec.15796 . https://do 10.1111/mec.15796 http://dx.doi.org/10.1111/mec.15796

Offret C , Gauthier O , Despréaux G et al . 2023 . Microbiota of the digestive glands and extrapallial fluids of clams evolve differently over time depending on the intertidal position . Microbial Ecology , 85 ( 1 ): 288 - 297 , https://doi.org/10.1007/s00248-022-01959-0 https://doi.org/10.1007/s00248-022-01959-0 .

Petton B , Destoumieux-Garzón D , Pernet F et al . 2021 . The Pacific Oyster Mortality Syndrome, a polymicrobial and multifactorial disease: state of knowledge and future directions . Frontiers in Immunology , 12 : 630343 , https://doi.org/10.3389/fimmu.2021.630343 https://doi.org/10.3389/fimmu.2021.630343 .

Pierce M L , Ward J E . 2018 . Microbial ecology of the Bivalvia, with an emphasis on the family Ostreidae . Journal of Shellfish Research , 37 ( 4 ): 793 - 806 , https://doi.org/10.2983/035.037.0410 https://doi.org/10.2983/035.037.0410 .

Pimentel Z T , Dufault-Thompson K , Russo K T et al . 2021 . Microbiome analysis reveals diversity and function of Mollicutes associated with the Eastern oyster, Crassostrea virginica . mSphere , 6 ( 3 ): e00227 - 21 , https://doi.org/10.1128/mSphere.00227-21 https://doi.org/10.1128/mSphere.00227-21 .

Rasmussen J A , Villumsen K R , Duchêne D A et al . 2021 . Genome-resolved metagenomics suggests a mutualistic relationship between Mycoplasma and salmonid hosts . Communications Biology , 4 ( 1 ): 579 , https://doi.‍org/10.1038/s42003-021-02105-1 https://doi.‍org/10.1038/s42003-021-02105-1 . https://do 10.1038/s42003-021-02105-1 http://dx.doi.org/10.1038/s42003-021-02105-1

Relman D A . 2012 . The human microbiome: ecosystem resilience and health . Nutrition Reviews , 70 ( S1 ): S2 - S9 , https://doi.org/10.1111/j.1753-4887.2012.00489.x https://doi.org/10.1111/j.1753-4887.2012.00489.x .

Rosenberg E , Koren O , Reshef L et al . 2007 . The role of microorganisms in coral health, disease and evolution . Nature Reviews Microbiology , 5 ( 5 ): 355 - 362 , https://doi.org/10.1038/nrmicro1635 https://doi.org/10.1038/nrmicro1635 .

Scanes E , Parker L M , Seymour J R et al . 2021 . Climate change alters the haemolymph microbiome of oysters . Marine Pollution Bulletin , 164 : 111991 , https://doi.org/10.1016/j.marpolbul.2021.111991 https://doi.org/10.1016/j.marpolbul.2021.111991 .

Schmitt P , Rosa R D , Duperthuy M et al . 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 , https://doi.‍org/10.3389/fmicb.2012.00160 https://doi.‍org/10.3389/fmicb.2012.00160 . https://do 10.3389/fmicb.2012.00160 http://dx.doi.org/10.3389/fmicb.2012.00160

Shade A , Peter H , Allison S D et al . 2012 . Fundamentals of microbial community resistance and resilience . Frontiers in Microbiology , 3 : 417 , https://doi.org/10.3389/fmicb.2012.00417 https://doi.org/10.3389/fmicb.2012.00417 .

Shang Q S , Shan X D , Cai C et al . 2016 . Dietary fucoidan modulates the gut microbiota in mice by increasing the abundance of Lactobacillus and Ruminococcaceae . Food & Function , 7 ( 7 ): 3224 - 3232 , https://doi.‍org/10.1039/c6fo00309e https://doi.‍org/10.1039/c6fo00309e . https://do 10.1039/c6fo00309e http://dx.doi.org/10.1039/c6fo00309e

Shannon P , Markiel A , Ozier O et al . 2003 . Cytoscape: a software environment for integrated models of biomolecular interaction networks . Genome Research , 13 ( 11 ): 2498 - 2504 , https://doi.org/10.1101/gr.1239303 https://doi.org/10.1101/gr.1239303 .

Solomieu V B , Renault T , Travers M A . 2015 . Mass mortality in bivalves and the intricate case of the Pacific oyster, Crassostrea gigas . Journal of Invertebrate Pathology , 131 : 2 - 10 , https://doi.org/10.1016/j.jip.2015.07.011 https://doi.org/10.1016/j.jip.2015.07.011 .

Unzueta-Martínez A , Welch H , Bowen J L . 2022 . Determining the composition of resident and transient members of the oyster microbiome . Frontiers in Microbiology , 12 : 828692 , https://doi.‍org/10.3389/fmicb.2021.828692 https://doi.‍org/10.3389/fmicb.2021.828692 . https://do 10.3389/fmicb.2021.828692 http://dx.doi.org/10.3389/fmicb.2021.828692

van de Water J A J M , Melkonian R , Junca H et al . 2016 . Spirochaetes dominate the microbial community associated with the red coral Corallium rubrum on a broad geographic scale . Scientific Reports , 6 : 27277 , https://doi.org/10.1038/srep27277 https://doi.org/10.1038/srep27277 .

Vanhoutte T , Huys G , Brandt E et al . 2004 . Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers . FEMS Microbiology Ecology , 48 ( 3 ): 437 - 446 , https://doi.‍org/10.1016/j.femsec.2004.03.001 https://doi.‍org/10.1016/j.femsec.2004.03.001 . https://do 10.1016/j.femsec.2004.03.001 http://dx.doi.org/10.1016/j.femsec.2004.03.001

Wang L L , Song X R , Song L S . 2018 . The oyster immunity . Developmental & Comparative Immunology , 80 : 99 - 118 , https://doi.org/10.1016/j.dci.2017.05.025 https://doi.org/10.1016/j.dci.2017.05.025 .

Wang Y , Huang J M , Wang S L et al . 2016 . Genomic characterization of symbiotic mycoplasmas from the stomach of deep-sea isopod Bathynomus sp . Environmental Microbiology , 18 ( 8 ): 2646 - 2659 , https://doi.org/10.1111/1462-2920.13411 https://doi.org/10.1111/1462-2920.13411 .

Watermann B T , Herlyn M , Daehne B et al . 2008 . Pathology and mass mortality of Pacific oysters, Crassostrea gigas (Thunberg), in 2005 at the East Frisian coast, Germany . Journal of Fish Diseases , 31 ( 8 ): 621 - 630 , https://doi.org/10.1111/j.1365-2761.2008.00953.x https://doi.org/10.1111/j.1365-2761.2008.00953.x .

Zhang L S , Wang X D , Zhang W Q et al . 2022 . Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas . Journal of Oceanology and Limnology , 40 ( 2 ): 620 - 633 , https://doi.org/10.1007/s00343-021-0462-x https://doi.org/10.1007/s00343-021-0462-x .

Zhou J Z , Deng Y , Luo F et al . 2010 . Functional molecular ecological networks . mBio , 1 ( 4 ): e00169 - 10 , https://doi.org/10.1128/mBio.00169-10 https://doi.org/10.1128/mBio.00169-10 .

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Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas

Spatial compartmentalization and temporal stability of associated microbiota in Pacific oyster Crassostrea gigas

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摘要

Abstract

关键词

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