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Inter-individual variability in copepod microbiomes reveals bacterial networks linked to host physiology

The ISME Journal (2018) | Download Citation


Copepods harbor diverse bacterial communities, which collectively carry out key biogeochemical transformations in the ocean. However, bulk copepod sampling averages over the variability in their associated bacterial communities, thereby limiting our understanding of the nature and specificity of copepod–bacteria associations. Here, we characterize the bacterial communities associated with nearly 200 individual Calanus finmarchicus copepods transitioning from active growth to diapause. We find that all individual copepods sampled share a small set of “core” operational taxonomic units (OTUs), a subset of which have also been found associated with other marine copepod species in different geographic locations. However, most OTUs are patchily distributed across individual copepods, thereby driving community differences across individuals. Among patchily distributed OTUs, we identified groups of OTUs correlated with common ecological drivers. For instance, a group of OTUs positively correlated with recent copepod feeding served to differentiate largely active growing copepods from those entering diapause. Together, our results underscore the power of individual-level sampling for understanding host–microbiome relationships.

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  1. 1.

    Turner JT. The importance of small planktonic copepods and their roles in Pelagic marine food webs. Zool Stud. 2004;43:255–66.

  2. 2.

    Jónasdóttir SH, Visser AW, Richardson K, Heath MR. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. Proc Natl Acad Sci USA 2015;2015:12110.

  3. 3.

    Møller EF, Riemann L, Søndergaard M. Bacteria associated with copepods: abundance, activity and community composition. Aquat Microb Ecol. 2007;47:99–106.

  4. 4.

    Sochard MR, Wilson DF, Austin B, Colwell RR. Bacteria associated with the surface and gut of marine copepods. Appl Environ Microbiol. 1979;37:750–9.

  5. 5.

    Tang KW, Turk V, Grossart HP. Linkage between crustacean zooplankton and aquatic bacteria. Aquat Microb Ecol. 2010;61:261–77.

  6. 6.

    De Corte D, Lekunberri I, Sintes E, Garcia J, Gonzales S, Herndl GJ. Linkage between copepods and bacteria in the North Atlantic Ocean. Aquat Microb Ecol. 2014;72:215–25.

  7. 7.

    Scavotto RE, Dziallas C, Bentzon-Tilia M, Riemann L, Moisander PH. Nitrogen-fixing bacteria associated with copepods in coastal waters of the North Atlantic Ocean. Environ Microbiol. 2015;17:3754–65.

  8. 8.

    Tang KW, Glud RN, Glud A, Rysgaard S, Nielsen TG. Copepod guts as biogeochemical hotspots in the sea: evidence from microelectrode profiling of Calanus spp. Limnol Oceanogr. 2011;56:666–72.

  9. 9.

    Turner JT. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr. 2015;130:205–48.

  10. 10.

    Bickel SL, Tang KW. Carbon substrate usage by zooplankton-associated bacteria, phytoplankton-associated bacteria, and free-living bacteria under aerobic and anaerobic conditions. Mar Biol. 2014;161:2233–42.

  11. 11.

    Bickel SL, Tang KW. Microbial decomposition of proteins and lipids in copepod versus rotifer carcasses. Mar Biol. 2010;157:1613–24.

  12. 12.

    Tang KW. Copepods as microbial hotspots in the ocean: effects of host feeding activities on attached bacteria. Aquat Microb Ecol. 2005;38:31–40.

  13. 13.

    Møller EF, Thor P, Nielsen TG. Production of DOC by Calanus finmarchicus, C. glacialis and C. hyperboreus through sloppy feeding and leakage from fecal pellets. Mar Ecol Prog Ser. 2003;262:185–91.

  14. 14.

    Carman KR, Dobbs FC. Epibiotic microorganisms on copepods and other marine crustaceans. Microsc Res Tech. 1997;37:116–35.

  15. 15.

    Grossart H-P, Dziallas C, Leunert F, Tang KW. Bacteria dispersal by hitchhiking on zooplankton. Proc Natl Acad Sci USA. 2010;107:11959–64.

  16. 16.

    Cordero OX, Datta MS. Microbial interactions and community assembly at microscales. Curr Opin Microbiol. 2016;31:227–34.

  17. 17.

    Baumgartner MF, Tarrant AM. The physiology and ecology of diapause in marine copepods. Annu Rev Mar Sci. 2017;9:387–411.

  18. 18.

    Gislason A, Silva T. Abundance, composition, and development of zooplankton in the Subarctic Iceland Sea in 2006, 2007, and 2008. ICES J Mar Sci. 2012;69:1263–76.

  19. 19.

    Heath M, Boyle P, Gislason A, Gurney W, Hay S, Head E, et al. Comparative ecology of over-wintering Calanus finmarchicus in the northern North Atlantic, and implications for life-cycle patterns. ICES J Mar Sci. 2004;61:698–708.

  20. 20.

    Hirche H-J. Overwintering of Calanus finmarchicus and Calanus helgolandicus. Mar Ecol Prog Ser. 1983;11:281–90.

  21. 21.

    Hirche H-J. Spatial distribution of digestive enzyme activities of Calanus finmarchicus and C.hyperboreus in Fram Strait/Greenland Sea. J Plankton Res. 1989;11:431–43.

  22. 22.

    Miller CB, Cowles TJ, Wiebe PH, Copley NJ, Grigg H. Phenology in Calanus finmarchicus; hypotheses about control mechanisms. 1991. (accessed March 28, 2016).

  23. 23.

    Arashkevich EG, Tande KS, Pasternak AF, Ellertsen B. Seasonal moulting patterns and the generation cycle of Calanus finmarchicus in the NE Norwegian Sea, as inferred from gnathobase structures, and the size of gonads and oil sacs. Mar Biol. 2004;146:119–32.

  24. 24.

    Sartoris FJ, Thomas DN, Cornils A, Schnack-Schiel SB. Buoyancy and diapause in Antarctic copepods: the role of ammonium accumulation. Limnol Oceanogr. 2010;55:1860–4.

  25. 25.

    Schrunder S, Schnack-Schiel SB, Auel H, Sartoris FJ. Control of diapause by acidic pH and ammonium accumulation in the hemolymph of Antarctic copepods. PLoS ONE. 2013;8:e77498.

  26. 26.

    Tarrant AM, Baumgartner MF, Hansen BH, Altin D, Nordtug T, Olsen AJ. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus. Front Zool. 2014;11:1.

  27. 27.

    Tarrant AM, Baumgartner MF, Verslycke T. Differential gene expression in diapausing and active Calanus finmarchicus (Copepoda). Mar Ecol Prog Ser. 2008;355:193–207.

  28. 28.

    Aruda AM, Baumgartner MF, Reitzel AM, Tarrant AM. Heat shock protein expression during stress and diapause in the marine copepod Calanus finmarchicus. J Insect Physiol. 2011;57:665–75.

  29. 29.

    Miller CB, Crain JA, Morgan CA. Oil storage variability in Calanus finmarchicus. ICES J Mar Sci J Cons. 2000;57:1786–99.

  30. 30.

    Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol. 2010;8:593–9.

  31. 31.

    Moisander PH, Sexton AD, Daley MC. Stable associations masked by temporal variability in the marine copepod microbiome. PloS ONE. 2015;10:e0138967.

  32. 32.

    Shoemaker KM, Moisander PH (2015). Microbial diversity associated with copepods in the North Atlantic subtropical gyre. FEMS Microbiol Ecol.

  33. 33.

    Urbanczyk H, Ogura Y, Hayashi T. Taxonomic revision of Harveyi clade bacteria (family Vibrionaceae) based on analysis of whole genome sequences. Int J Syst Evol Microbiol. 2013;63:2742–51.

  34. 34.

    Klindworth A,Pruesse E,Schweer T,Peplies J,Quast C,Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1

  35. 35.

    Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol. 2014;12:635–45.

  36. 36.

    Gerdts G, Brandt P, Kreisel K, Boersma M, Schoo KL, Wichels A. The microbiome of North Sea copepods. Helgol Mar Res. 2013;67:757–73.

  37. 37.

    Aitchison J. The statistical analysis of compositional data. London, New York: Chapman and Hall; 1986.

  38. 38.

    Raftery AE. Bayesian model selection in social research. Sociol Methodol. 1995;25:111.

  39. 39.

    Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.

  40. 40.

    Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol. 2014;12:686–98.

  41. 41.

    Riddle MR, Baxter BK, Avery BJ. Molecular identification of microorganisms associated with the brine shrimp Artemia franciscana. Aquat Biosyst. 2013;9:7.

  42. 42.

    Ohman MD, Runge JA. Sustained fecundity when phytoplankton resources are in short supply: omnivory by Calanus finmarchicus in the Gulf of St. Lawrence. Limnol Oceanogr. 1994;39:21–36.

  43. 43.

    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinforma Oxf Engl. 2010;26:2460–1.

  44. 44.

    Pruesse E, Peplies J, Glockner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.

  45. 45.

    Price MN, Dehal PS, Arkin AP. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.

  46. 46.

    Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.

  47. 47.

    Fruchterman TMJ, Reingold EM. Graph drawing by force-directed placement. Softw Pract Exp. 1991;21:1129–64.

  48. 48.

    Tang KW, Bickel SL, Dziallas C, Grossart HP. Microbial activities accompanying decomposition of cladoceran and copepod carcasses under different environmental conditions. Aquat Microb Ecol 2009;57:89–100.

  49. 49.

    Zhou J, Bruns MA, Tiedje JM. DNA recovery from soils of diverse composition. Appl Environ Microbiol 1996;62:316–322.

  50. 50.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537–7541.

  51. 51.

    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Appl Environ Microbiol 2007;73:5261–5267.

  52. 52.

    Preheim SP, Perrotta AR, Martin-Platero AM, Gupta A, Alm EJ. Distribution-based clustering: using ecology to refine the operational taxonomic unit. Appl Environ Microbiol 2013;79:6593–6603.

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This work was supported in part by National Science Foundation grants OCE-1132567 to MFB and AMT and OCE-1435993 to MFP. MSD was supported by the Department of Defense through the National Defense Science and Engineering Graduate (NDSEG) Fellowship program. AAA was supported by an EPA STAR Fellowship, NSF GRFP, and the WHOI Ocean Venture Fund. We thank Sarah Preheim for help with performing the distribution-based clustering, Michael Cutler for providing advice regarding 16S rRNA library preparation, Nadine Lysiak for assistance in the field, Morgan Rubanow for assistance with the morphometric analysis, Krista Longnecker for her advice regarding the bacterial abundance counts, Bjørn Henrik Hansen, Dag Altin, Trond Nordtug, and Anders Olsen for significant logistical support in Trondheim, Norway, and the captain and crew of the R/V Gunnerus.

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Author notes

  1. These authors contributed equally: Manoshi S. Datta, Amalia A. Almada


  1. Computational and Systems Biology Graduate Program, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA

    • Manoshi S. Datta
  2. Biology Department, Woods Hole Oceanographic Institution, 45 Water Street, Woods Hole, MA, 02543, USA

    • Amalia A. Almada
    • , Mark F. Baumgartner
    • , Tracy J. Mincer
    •  & Ann M. Tarrant
  3. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA

    • Martin F. Polz


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Correspondence to Martin F. Polz.

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