Microbiota of the Digestive Glands and Extrapallial Fluids of Clams Evolve Differently Over Time Depending on the Intertidal Position.

Clam Digestive gland Extrapallial fluids Microbiota Temporal variations

Journal

Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663

Informations de publication

Date de publication:
Jan 2023
Historique:
received: 15 10 2021
accepted: 04 01 2022
pubmed: 24 1 2022
medline: 21 1 2023
entrez: 23 1 2022
Statut: ppublish

Résumé

The Manila clam (Ruditapes philippinarum) is the second most exploited bivalve in the world but remains threatened by diseases and global changes. Their associated microbiota play a key role in their fitness and acclimation capacities. This study aimed at better understanding the behavior of clam digestive glands and extrapallial fluids microbiota at small, but contrasting spatial and temporal scales. Results showed that environmental variations impacted clam microbiota differently according to the considered tissue. Each clam tissue presented its own microbiota and showed different dynamics according to the intertidal position and sampling period. Extrapallial fluids microbiota was modified more rapidly than digestive glands microbiota, for clams placed on the upper and lower intertidal position, respectively. Clam tissues could be considered as different microhabitats for bacteria as they presented different responses to small-scale temporal and spatial variabilities in natural conditions. These differences underlined a more stringent environmental filter capacity of the digestive glands.

Identifiants

pubmed: 35066615
doi: 10.1007/s00248-022-01959-0
pii: 10.1007/s00248-022-01959-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

288-297

Subventions

Organisme : Agence Nationale de la Recherche
ID : ANR-17-EURE-0015
Organisme : Horizon 2020
ID : 678589
Organisme : Région Bretagne
ID : 2017-Stratégie d'Attractivité Durable

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Weissenbach J, Sghir A (2016) Microbiotes and metagenomics. Med Sci: M/S 32:937–943
Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci 101:4596–4601
doi: 10.1073/pnas.0400706101
Rosenberg E, Koren O, Reshef L et al (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362. https://doi.org/10.1038/nrmicro1635
doi: 10.1038/nrmicro1635
Dishaw LJ, Cannon JP, Litman GW, Parker W (2014) Immune-directed support of rich microbial communities in the gut has ancient roots. Dev Comp Immunol 47:36–51
doi: 10.1016/j.dci.2014.06.011
Gil-Agudelo DL, Myers C, Smith GW, Kim K (2006) Changes in the microbial communities associated with Gorgonia ventalina during aspergillosis infection. Dis Aquat Org 69:89–94
doi: 10.3354/dao069089
Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259
doi: 10.1128/AEM.00554-06
Littman RA, Willis BL, Pfeffer C, Bourne DG (2009) Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68:152–163
doi: 10.1111/j.1574-6941.2009.00666.x
Chen C-P, Tseng C-H, Chen CA, Tang S-L (2011) The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5:728–740
doi: 10.1038/ismej.2010.151
Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25:195–231. https://doi.org/10.1007/BF00171889
doi: 10.1007/BF00171889
Sakowski EG (2015) The microbiome of the eastern oyster, Crassostrea virginica, in health and disease. University of Delaware, Thesis
Offret C, Paulino S, Gauthier O, et al (2020) The marine intertidal zone shapes oyster and clam digestive bacterial microbiota. FEMS Microbiology Ecology 96 https://doi.org/10.1093/femsec/fiaa078
Lokmer A, Wegner KM (2014) Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. ISME J 9:670–682. https://doi.org/10.1038/ismej.2014.160
doi: 10.1038/ismej.2014.160
Cúcio C, Engelen AH, Costa R, Muyzer G (2016) Rhizosphere microbiomes of European seagrasses are selected by the plant, but are not species specific. Front Microbiol 7:440
doi: 10.3389/fmicb.2016.00440
Sharp KH, Pratte ZA, Kerwin AH et al (2017) Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata. Microbiome 5:120
doi: 10.1186/s40168-017-0329-8
Woo S, Yang S-H, Chen H-J et al (2017) Geographical variations in bacterial communities associated with soft coral Scleronephthya gracillimum. PLoS One 12:e0183663. https://doi.org/10.1371/journal.pone.0183663
doi: 10.1371/journal.pone.0183663
Vijayan N, Lema KA, Nedved BT, Hadfield MG (2019) Microbiomes of the polychaete Hydroides elegans (Polychaeta: Serpulidae) across its life-history stages. Mar Biol 166:19. https://doi.org/10.1007/s00227-019-3465-9
doi: 10.1007/s00227-019-3465-9
Trabal Fernández N, Mazón-Suástegui JM, Vázquez-Juárez R et al (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. https://doi.org/10.1111/1574-6941.12270
doi: 10.1111/1574-6941.12270
Pierce ML, Ward JE (2019) Gut microbiomes of the eastern oyster ( Crassostrea virginica ) and the blue mussel ( Mytilus edulis ): temporal variation and the influence of marine aggregate-associated microbial communities. mSphere 4:e00730–19, /msphere/4/6/mSphere730–19.atom. https://doi.org/10.1128/mSphere.00730-19
King WL, Siboni N, Kahlke T, et al (2020) Regional and oyster microenvironmental scale heterogeneity in the Pacific oyster bacterial community. FEMS Microbiol Ecol 96 https://doi.org/10.1093/femsec/fiaa054
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. https://doi.org/10.1111/1751-7915.13277
doi: 10.1111/1751-7915.13277
Meisterhans G, Raymond N, Girault E et al (2016) Structure of Manila clam (Ruditapes philippinarum) microbiota at the organ scale in contrasting sets of individuals. Microb Ecol 71:194–206. https://doi.org/10.1007/s00248-015-0662-z
doi: 10.1007/s00248-015-0662-z
Milan M, Carraro L, Fariselli P et al (2018) Microbiota and environmental stress: how pollution affects microbial communities in Manila clams. Aquat Toxicol 194:195–207. https://doi.org/10.1016/j.aquatox.2017.11.019
doi: 10.1016/j.aquatox.2017.11.019
Leite L, Jude-Lemeilleur F, Raymond N et al (2017) Phylogenetic diversity and functional characterization of the Manila clam microbiota: a culture-based approach. Environ Sci Pollut Res 24:21721–21732. https://doi.org/10.1007/s11356-017-9838-z
doi: 10.1007/s11356-017-9838-z
Allam B, Pales Espinosa E (2016) Bivalve immunity and response to infections: are we looking at the right place? Fish Shellfish Immunol 53:4–12. https://doi.org/10.1016/j.fsi.2016.03.037
doi: 10.1016/j.fsi.2016.03.037
Lavaud R, Artigaud S, Le Grand F et al (2018) New insights into the seasonal feeding ecology of Pecten maximus using pigments, fatty acids and sterols analyses. Mar Ecol Prog Ser 590:109–129
doi: 10.3354/meps12476
Lee R, Lovatelli A, Ababouch L (2008) Bivalve depuration: fundamental and practical aspects. Food and Agriculture Organization of the United Nations
Herlemann DP, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
doi: 10.1038/ismej.2011.41
Escudié F, Auer L, Bernard M et al (2018) FROGS: Find, Rapidly, OTUs with Galaxy Solution. Bioinformatics 34:1287–1294. https://doi.org/10.1093/bioinformatics/btx791
doi: 10.1093/bioinformatics/btx791
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
doi: 10.1093/bioinformatics/btr507
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal 17:10–12
doi: 10.14806/ej.17.1.200
Mahé F, Rognes T, Quince C et al (2014) Swarm: robust and fast clustering method for amplicon-based studies. PeerJ 2:e593
doi: 10.7717/peerj.593
Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
doi: 10.1093/bioinformatics/btr381
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
doi: 10.7717/peerj.2584
Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. https://doi.org/10.1038/nmeth.2276
doi: 10.1038/nmeth.2276
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421
doi: 10.1186/1471-2105-10-421
Quast C, Pruesse E, Yilmaz P et al (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596
doi: 10.1093/nar/gks1219
Legendre P, Borcard D (2018) Box–Cox-chord transformations for community composition data prior to beta diversity analysis. Ecography 41:1820–1824
doi: 10.1111/ecog.03498
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297. https://doi.org/10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2
doi: 10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2
Team RC (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2012. URL http://www.R-project.org
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS one 8:e61217
doi: 10.1371/journal.pone.0061217
Oksanen J, Blanchet FG, Friendly M, et al (2019) vegan: Community Ecology Package
Lenth R, Buerkner P, Herve M, et al (2020) Emmeans: estimated marginal means, aka Least-Squares Means
Chen W, Simpson J, Levesque CA (2016) RAM: R for amplicon-sequencing-based microbial-ecology. R package version 1:
Kowarik A, Templ M (2016) Imputation with the R package VIM. J Stat Softw 74:1–16
doi: 10.18637/jss.v074.i07
WILBUR KM, Saleuddin ASM (1983) Shell formation. In: The mollusca. Elsevier, pp 235–287
Allam B, Paillard C (1998) Defense factors in clam extrapallial fluids. Dis Aquat Org 33:123–128. https://doi.org/10.3354/dao033123
doi: 10.3354/dao033123
Lokmer A, Goedknegt MA, Thieltges DW, et al (2016) Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales. Front Microbiol 7 https://doi.org/10.3389/fmicb.2016.01367

Auteurs

Clément Offret (C)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France.

Olivier Gauthier (O)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France.

Garance Despréaux (G)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France.

Adeline Bidault (A)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France.

Charlotte Corporeau (C)

Ifremer, Univ Brest, CNRS, IRD, LEMAR, Plouzané, 29280, Brest, France.

Philippe Miner (P)

Ifremer, Univ Brest, CNRS, IRD, LEMAR, Plouzané, 29280, Brest, France.

Bruno Petton (B)

Ifremer, Univ Brest, CNRS, IRD, LEMAR, Plouzané, 29280, Brest, France.

Fabrice Pernet (F)

Ifremer, Univ Brest, CNRS, IRD, LEMAR, Plouzané, 29280, Brest, France.

Caroline Fabioux (C)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France.

Christine Paillard (C)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France.

Gwenaelle Le Blay (G)

Univ Brest, CNRS, IRD, Ifremer, LEMAR, F-29280, Plouzané, France. gwenaelle.leblay@univ-brest.fr.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH