Skip to main content

Advertisement

Springer Nature Link
Log in

The influence of site and season on the gut and pallial fluid microbial communities of the eastern oyster, Crassostrea virginica (Bivalvia, Ostreidae): community-level physiological profiling and genetic structure

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The microbial communities and overall health of the eastern oyster, Crassostrea virginica, have long been topics of interest due to the fundamental economic and ecological roles this species maintains. A broad scale characterization of the oyster microbiome over spatial and seasonal scales, however, has never been carried out. The primary goal of this study was to examine the factors mediating microbial communities of the gut and pallial fluid of C. virginica at three sites within the Long Island Sound estuary, with a focus on both genetic structure (T-RFLP) and physiological profiling (EcoPlates) of the microbiome. Results indicated that the genetic structure of microbial communities of oysters was minimally separated across sites, but was influenced by season. Although the microbial community structure was similar, the number of carbon sources utilized by these communities (richness) varied across site, season, and anatomical location within the host. Parameters including oyster condition index, Dermo disease, and ambient water temperature were measured to assess their influence on the oyster microbiome. Only water temperature was found to have a significant relationship with microbial community structure and richness. Results suggest that a core microbiome may exist within the eastern oyster, specifically for those populations that are not genetically distinct.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Bayne, B. L. & R. C. Newell, 1983. Physiological energetics of marine molluscs. In Saleuddin, S. M. & K. M. Wilbur (eds), The Mollusca Volume 4: Physiology, Part 1, Vol. 4. Academic Press Ltd, London: 407–499.

    Chapter  Google Scholar 

  • Bickel, S. L., K. W. Tang & H. P. Grossart, 2014. Structure and function of zooplankton-associated bacterial communities in a temperate estuary change more with time than with zooplankton species. Aquatic Microbial Ecology 72: 1–15.

    Article  Google Scholar 

  • Blackwood, C. B., T. Marsh, S. Kim & E. A. Paul, 2003. Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities. Applied Environmental Microbiology 69: 926–932.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Breitbart, M., R. Bhagooli, S. Griffin, I. Johnston & F. Rohwer, 2005. Microbial communities associated with skeletal tumors on Porites compressa. FEMS Microbiology Letters 243: 431–436.

    Article  CAS  PubMed  Google Scholar 

  • Brettar, I., R. Christen & M. G. Höfle, 2004. Aquiflexum balticum gen. nov., sp. Nov, a novel marine bacterium of the Cytophaga–Flavobacterium–Bacteroides group isolated from surface water of the central Baltic Sea. International Journal of Systematic and Evolutionary Microbiology 54: 2335–2341.

    Article  CAS  PubMed  Google Scholar 

  • Cavallo, R. A., M. I. Acquaviva & L. Stabili, 2009. Culturable heterotrophic bacteria in seawater and Mytilus galloprovincialis from a Mediterranean area (Northern Ionian Sea–Italy). Environmental Monitoring and Assessment 149: 465–475.

    Article  CAS  PubMed  Google Scholar 

  • Colorni, A., 1985. A study on the bacterial flora of giant prawn Macrobrachium rosenbergii, larvae fed with Artemia salina nauplii. Aquaculture 9: 1–10.

    Article  Google Scholar 

  • Colwell, R. R. & J. Liston, 1960. Microbiology of shellfish: bacteriological study of the natural flora of Pacific Oysters (Crassostrea gigas). Journal of Applied Microbiology 8: 104–109.

    CAS  Google Scholar 

  • Colwell, R. R. & A. K. Sparks, 1967. Properties of Pseudomonas enalia, a marine bacterium pathogenic for the invertebrate Crassostrea gigas (Thunberg). Journal of Applied Microbiology 15(5): 980–986.

    CAS  Google Scholar 

  • Comte, J., F. Fauteux & P. A. del Giorgio, 2013. Links between metabolic plasticity and functional redundancy in freshwater bacterioplankton communities. Frontiers in Microbiology. doi:10.3389/fmicb.2013.00112.

    PubMed Central  PubMed  Google Scholar 

  • Crosby, M. P. & L. D. Gale, 1990. A review and evaluation of bivalve condition index methodologies with a suggested standard method. Journal of Shellfish Research 9(1): 233–237.

    Google Scholar 

  • Crosby, M. P., R. I. E. Newell & C. J. Langdon, 1990. Bacterial mediation in the utilization of carbon and nitrogen from detrital complexes by Crassostrea virginica. Limnology and Oceanography 35: 625–639.

    Article  CAS  Google Scholar 

  • Culman, S. W., H. G. Gauch, S. B. Blackwood & J. E. Thies, 2008. Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. Journal of Microbiological Methods 75: 55–63.

    Article  CAS  PubMed  Google Scholar 

  • Daims, H., A. Brühl, R. Amann, K. H. Schleifer & M. Wagner, 1999. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology 22: 434–444.

    Article  CAS  PubMed  Google Scholar 

  • Deming, J. W., P. S. Tabor & R. R. Colwell, 1981. Barophilic growth of bacteria from intestinal tracts of deep-sea invertebrates. Microbial Ecology 7: 85–94.

    Article  CAS  PubMed  Google Scholar 

  • DePaola, A., L. H. Hopkins, J. T. Peeler, B. Wentz & R. M. McPhearson, 1990. Incidence of Vibrio parahaemolyticus in US coastal waters and oysters. Applied and Environmental Microbiology 56(8): 2299–2302.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dishaw, L. J., J. Flores-Torres, S. Lax, K. Gemayel, B. Leigh, D. Melillo, M. G. Mueller, L. Natale, I. Zucchetti, R. De Santis, M. R. Pinto, G. W. Litman & J. A. Gilbert, 2014a. The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS One 9: e93386.

    Article  PubMed Central  PubMed  Google Scholar 

  • Dishaw, L. J., J. P. Cannon, G. W. Litman & W. Parker, 2014b. Immune-directed support of rich microbial communities in the gut has ancient roots. Developmental and Comparative Immunology 47: 36–51.

    Article  PubMed Central  PubMed  Google Scholar 

  • Douglas, A. E., S. Bouvaine & R. R. Russell, 2011. How the insect immune system interacts with an obligate symbiotic bacterium. Proceedings of the Royal Society B: Biological Sciences 278: 333–338.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duchene, J. C., P. Imbaud & D. Delille, 1988. Associated bacterial microflora of a subantarctic polychaete worm Thelepus setosus. Archiv fuer Hydrobiologie 112: 221–231.

    Google Scholar 

  • Dunbar, J., L. O. Ticknor & C. R. Kuske, 2001. Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Applied and Environmental Microbiology 67: 190–197.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fan, L., D. Reynolds, M. Liu, M. Stark, S. Kjelleberg, N. S. Webster & T. Thomas, 2012. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proceedings of the National Academy of Sciences 109: E1878–E1887.

    Article  CAS  Google Scholar 

  • Frias-Lopez, J., A. L. Zerkl, G. T. Bonheyo & B. W. Fouke, 2002. Partitioning of bacterial communities between seawater and healthy, black band diseased and dead coral surfaces. Applied and Environmental Microbiology 68: 2214–2228.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gaffney, P. M., 1996. Biochemical and population genetics. In Kennedy, V. S., R. I. E. Newell & A. E. Eble (eds), The Eastern Oyster, Crassostrea virginica. Maryland Sea Grant, College Park: 423–441.

    Google Scholar 

  • Gillian, D. C., A. G. C. L. Speksnijder, G. Zwart & C. De Ridder, 1998. Genetic diversity of the biofilm covering Montacuta ferruginosa (Mollusca, Bivalvia) as evaluated by denaturing gradient gel electrophoresis analysis and cloning of PCR-amplified gene fragments coding for 16S rRNA. Applied and Environmental Microbiology 64(9): 3464–3472.

    Google Scholar 

  • Greenberg, A. E. & D. A. Hunt (eds), 1985. Laboratory Procedures for the Examination of Seawater and Shellfish, 5th ed. American Public Health Association, Washington, DC.

    Google Scholar 

  • Green, T. J. & A. C. Barnes, 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: 613–622.

    CAS  PubMed  Google Scholar 

  • Harris, J. M., 1993. The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microbial Ecology 25: 195–231.

    Article  CAS  PubMed  Google Scholar 

  • Harris, J. M., L. J. Seiderer & M. I. Lucas, 1991. Gut microflora of two saltmarsh detritivore Thalassinid prawns, Upogebia africana and Callianassa kraussi. Microbial Ecology 21: 63–82.

    Article  Google Scholar 

  • Hedgecock, D., 1994. Does variance in reproductive success limit effective population sizes of marine organisms? In Beaumont, A. R. (ed.), Genetics and Evolution of Aquatic Organisms. Chapman & Hall, London: 122–134.

    Google Scholar 

  • Hernández-Zárate, G. & J. Olmos-Soto, 2006. Identification of bacterial diversity in the oyster Crassostreagigas by fluorescent in situ hybridization and polymerase chain reaction. Journal of Applied Microbiology 100: 664–672.

    Article  PubMed  Google Scholar 

  • Insam, H. & M. Goberna, 2004. Use of biolog for the community level physiological profiling (CLPP) of environmental samples. In Kowalchuk, G. A., F. J. de Pruijn, I. M. Head, A. D. L. Akkermans & J. D. van Elsas (eds), Molecular Microbial Ecology Manual, Vol. 2, 2nd ed. Kluwer Academic, Dordrecht: 853–860.

    Google Scholar 

  • Kau, A. L., P. P. Ahern, N. W. Griffin, A. L. Goodman & J. I. Gordon, 2011. Human nutrition, the gut microbiome, and the immune system. Nature 474: 327–336.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kennedy, V. S., 1996. Biology of larvae and spat. In Kennedy, V. S., R. I. E. Newell & A. E. Eble (eds), The Eastern Oyster, Crassostrea virginica. Maryland Sea Grant, College Park: 371–411.

    Google Scholar 

  • King, G. M., C. Judd, C. R. Kuske & C. Smith, 2012. Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS One 7(12): e51475.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kirchman, D. L., 2002. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiological Ecology 39: 91–100.

    CAS  Google Scholar 

  • Kueh, C. S. W. & K. Y. Chan, 1985. Bacteria in bivalve shellfish with special reference to the oyster. Journal of Applied Bacteriology 59: 41–47.

    Article  CAS  PubMed  Google Scholar 

  • Lane, D. J., 1991. 16S/23S rRNA sequencing. In Stackebrandt, E. & M. Goodfellow (eds), Nucleic Acid Techniques in Bacterial Systematics. Wiley, New York: 115–148.

    Google Scholar 

  • La Valley, K. J., S. Jones, M. Gomez-Chiarri, J. Dealteris & M. Rice, 2009. Bacterial community profiling of the eastern oyster (Crassostrea virginica): comparison of culture-dependent and culture-independent outcomes. Journal of Shellfish Research 28: 827–835.

    Article  Google Scholar 

  • Ley, R. E., F. Backhed, P. Turnbaugh, C. A. Lozupone, R. D. Knight & J. I. Gordon, 2005. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences 102: 11070–11075.

    Article  CAS  Google Scholar 

  • Liu, W. T., T. L. Marsh, H. Cheng & L. J. Forney, 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Applied and Environmental Microbiology 63: 4516–4522.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lokmer, A. & K. M. Wegner, 2014. Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. The International Society for Microbial Ecology Journal. doi:10.1038/ismej.2014.160.

    Google Scholar 

  • Loy, A., F. Maixner, M. Wagner & M. Horn, 2007. ProbeBase – an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Research 35: D800–D804.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lyons, M. M., J. E. Ward, H. Gaff, R. E. Hicks, J. M. Drake & F. C. Dobbs, 2010. Theory of island biogeography on a microscopic scale: organic aggregates as islands for aquatic pathogens. Aquatic Microbial Ecology 60: 1–13.

    Article  Google Scholar 

  • Manz, W., R. Amann, W. Ludwig, M. Vancanneyt & K. H. Schleifer, 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Journal of Microbiology 142: 1097–1106.

    Article  CAS  Google Scholar 

  • Moeseneder, M. M., J. M. Arrieta, G. Muyzer, C. Winter & G. J. Herndl, 1999. Optimization of terminal-restriction fragment length polymorphism analysis for complex marine bacterioplankton communities and comparison with denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 65: 3518–3525.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Motes, M. L., A. DePaola, D. W. Cook, J. E. Veazey, J. C. Hunsucker, W. E. Garthright, R. J. Blodgett & S. J. Chirtel, 1998. Influence of water temperature and salinity on Vibrio vulnificus in Northern Gulf and Atlantic Coast oysters (Crassostrea virginica). Applied and Environmental Microbiology 64(4): 1459–1465.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Murchelano, R. A. & C. Brown, 1968. Bacteriological study of the natural flora of the eastern oyster, Crassostrea virginica. Journal of Invertebrate Pathology 11: 519–520.

    Article  Google Scholar 

  • National Marine Fisheries Service (NMFS), 2014. Annual Commercial Landing Statistics, Fisheries Statistics. [available on internet at http://www.st.nmfs.noaa.gov/commercial-fisheries/commercial-landings/annual-landings/index].

  • Newell, R. I. E., T. R. Fisher, R. R. Holyoke & J. C. Cornwell, 2005. Influence of eastern oysters on nitrogen and phosphorus regeneration in Chesapeake Bay. In Dame, R. F. & S. Olenin (eds), The Comparative Rates of Suspension Feeders in Ecosystems. Springer, Dordrecht: 93–120.

    Chapter  Google Scholar 

  • Olafsen, J. A., H. V. Mikkelsen, H. M. Giaever & G. H. Hansen, 1993. Indigenous bacteria in hemolymph and tissues of marine bivalves at low temperatures. Applied and Environmental Microbiology 59: 1848–1854.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Osborn, A. M., E. R. B. Moore & K. N. Timmis, 2000. An evaluation of terminal restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environmental Microbiology 2: 39–50.

    Article  CAS  PubMed  Google Scholar 

  • Pernthaler, J., F. O. Glöckner, W. Schönhuber & R. Amann, 2001. Fluorescence in situ hybridization with rRNA-targeted oligonucleotide probes. In Paul, J. (ed), Methods in Microbiology: Marine Microbiology, Vol. 30. Academic Press Ltd, London: 207–226.

    Chapter  Google Scholar 

  • Pierce, M. L., J. E. Ward & F. C. Dobbs, 2014. False positives in Biolog MT2™ and EcoPlates™ caused by calcium. Journal of Microbiological Methods 97: 20–24.

    Article  CAS  PubMed  Google Scholar 

  • Pujalte, M. J., M. Ortigosa, M. C. Macián & E. Garay, 1999. Aerobic and facultative anaerobic heterotrophic bacteria associated to Mediterranean oysters and seawater. International Microbiology 2: 259–266.

    CAS  PubMed  Google Scholar 

  • Ramatte, A., 2007. Multivariate analyses in microbial ecology. FEMS Microbiology Ecology 62: 142–160.

    Article  Google Scholar 

  • Ravindran, J., E. Kannapiran, B. Manikandan, K. Francis, S. Arora, E. Karunya, A. Kumar, S. K. Singh & J. Jose, 2013. UV-absorbing bacteria in coral mucus and their response to simulated temperature elevations. Coral Reefs 32: 1043–1050.

    Article  Google Scholar 

  • Ray, S. M., 1966. A review of the culture method for detecting Dermocystidium marinum with suggested modifications and precautions. Proceedings of the National Shellfisheries Association 54: 55–69.

    Google Scholar 

  • Rawls, J. F., B. S. Samuel & J. I. Gordon, 2004. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proceedings of the National Academy of Sciences 101(13): 4596–4601.

    Article  CAS  Google Scholar 

  • Ristori, C. A., S. T. Iaria, D. S. Gelli & I. N. G. Rivera, 2007. Pathogenic bacteria associated with oysters (Crassostrea brasiliana) and estuarine waters along the south coast of Brazil. International Journal of Environmental Health Research 17: 259–269.

    Article  CAS  PubMed  Google Scholar 

  • Roder, C., C. Arif, C. Daniels, E. Weil & C. R. Voolstra, 2014. Bacterial profiling of white plague disease across corals and oceans indicates a conserved and distinct disease microbiome. Molecular Ecology 23: 965–974.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rohwer, F., V. Seguritan, F. Azam & N. Knowlton, 2002. Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series 243: 1–10.

    Article  Google Scholar 

  • Romero, J., M. Garcia-Varela, J. P. Laclette & R. T. Espejo, 2002. Bacterial 16S rRNA gene analysis revealed that bacteria related to Arcobacter spp. constitute an abundant and common component of the oyster microbiota (Tiostrea chilensis). Microbial Ecology 44: 365–371.

    Article  CAS  PubMed  Google Scholar 

  • Round, L. A., 1914. Contributions to the Bacteriology of the Oyster: The Results of Experiments and Observations Made While Conducting an Investigation Directed and Authorized by the Commissioners of Shell Fisheries of the State of Rhode Island. E.L. Freeman Co., Providence.

    Google Scholar 

  • Saha, R., R. S. Donofrio, D. M. Goeres & S. T. Bagley, 2012. Rapid detection of rRNA group I pseudomonads in contaminated metalworking fluids and biofilm formation by fluorescent in situ hybridization. Applied Microbiology and Biotechnology 94: 799–808.

    Article  CAS  PubMed  Google Scholar 

  • Sala, M. M., M. Estrada & J. M. Gasol, 2006. Seasonal changes in the functional diversity of bacterioplankton in contrasting coastal environments of the NW Mediterranean. Aquatic Microbial Ecology 44: 1–9.

    Article  Google Scholar 

  • Schultz, G. E. & H. W. Ducklow, 2000. Changes in bacterioplankton metabolic capabilities along a salinity gradient in the York River estuary, Virginia, USA. Aquatic Microbial Ecology 22: 163–174.

    Article  Google Scholar 

  • Schütte, U. M., Z. Abdo, S. J. Bent, C. Shyu, C. J. Williams, J. D. Pierson & L. J. Forney, 2008. Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Applied Microbiology and Biotechnology 80: 365–380.

    Article  PubMed  Google Scholar 

  • Schwarz, J. R., A. A. Yayanos & R. R. Colwell, 1976. Metabolic activities of the intestinal microflora of a deep-sea invertebrate. Applied and Environmental Microbiology 31: 46–48.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stefanowicz, A. M., M. Niklińska & R. Laskowski, 2008. Metals affect soil bacterial and fungal functional diversity differently. Environmental Toxicology and Chemistry 27(3): 591–598.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Trabal, N., J. M. Mazón- Suástegui, R. Vázquez-Juárez, F. Ascencio-Valle & J. Romero, 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: 69–83.

    Article  Google Scholar 

  • Trindade-Silva, A. E., C. Rua, G. G. Z. Silva, B. A. Dutilh, A. P. B. Moreira, R. A. Edwards, E. Hajdu, G. Lobo Hajdu, A. T. Vasconcelos, R. G. S. Berlinck & F. L. Thompson, 2012. Taxonomic and functional microbial signatures of the endemic marine sponge Arenosclera brasiliensis. PLoS One 7(7): e39905.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Turnbaugh, P. J., R. E. Ley, M. Hamady, C. M. Fraser-Liggett, R. Knight & J. I. Gordon, 2007. The human microbiome project. Nature 449: 804–810.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Unkles, S. E., 1977. Bacterial flora of the sea urchin Echinus esculentus. Applied and Environmental Microbiology 34: 347–350.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zak, J. C., M. R. Willig, D. L. Moorhead & H. G. Wildman, 1994. Functional diversity of microbial communities: a quantitative approach. Soil Biology and Biochemistry 26(9): 1101–1108.

    Article  Google Scholar 

  • Zurel, D., Y. Benayahu, A. Or, A. Kovacs & U. Gophna, 2011. Composition and dynamics of the gill microbiota of an invasive Indo-Pacific oyster in the eastern Mediterranean Sea. Environmental Microbiology 13(6): 1467–1476.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Norm and James Bloom of Norm Bloom and Son in Norwalk, CT and James Markow of The Noank Aquaculture Cooperative in Noank, CT for their generous help in collecting oysters. We also thank two anonymous reviewers for their valuable comments and work toward improving this manuscript. This research was supported by grants from the National Science Foundation, Ecology and Evolution of Infectious Diseases program to JEW (EF-0914459) and REH (EF-0914450). Support was also provided by a grant from NOAA’s Oceans and Human Health Initiative for the Interdisciplinary Research and Training Initiative on Coastal Ecosystems and Human Health (I-RICH) to JEW.

Author information

Authors and Affiliations

  1. Department of Marine Sciences, University of Connecticut, Avery Point, 1080 Shennecossett Rd., Groton, CT, 06340, USA

    Melissa L. Pierce, J. Evan Ward & Bridget A. Holohan

  2. Department of Biology, University of Minnesota Duluth, 1035 Kirby Drive, SSB 207, Duluth, MN, 55812, USA

    Xiaowei Zhao & Randall E. Hicks

Authors
  1. Melissa L. Pierce
    View author publications

    Search author on:PubMed Google Scholar

  2. J. Evan Ward
    View author publications

    Search author on:PubMed Google Scholar

  3. Bridget A. Holohan
    View author publications

    Search author on:PubMed Google Scholar

  4. Xiaowei Zhao
    View author publications

    Search author on:PubMed Google Scholar

  5. Randall E. Hicks
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Melissa L. Pierce.

Additional information

Handling editor: Diego Fontaneto

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 250 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pierce, M.L., Ward, J.E., Holohan, B.A. et al. The influence of site and season on the gut and pallial fluid microbial communities of the eastern oyster, Crassostrea virginica (Bivalvia, Ostreidae): community-level physiological profiling and genetic structure. Hydrobiologia 765, 97–113 (2016). https://doi.org/10.1007/s10750-015-2405-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2405-z

Keywords