Log in

Eukaryotic microbial richness increases with latitude and decreasing temperature in the Pacific Subarctic domain in late winter

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The Bering Sea has some of the highest concentrations of inorganic nutrients of any marine system. In the Bering Sea, eukaryotic microbes interface inorganic nutrient sequestration and cycling processes that drive one of the most productive ecosystems globally. Historical surveys of eukaryotic microbial diversity in the Bering Sea have relied on microscopy and culturing-dependent analyses to assess microbial diversity patterns. In this study, we used high-throughput sequencing (Illumina MiSeq) of the 18S rRNA gene to explore general patterns of eukaryotic microbial diversity from six regions in the Bering Sea and surrounding Subarctic Pacific. The greatest richness was found in the Shelikof Strait and at the marginal ice zone. The lowest richness was found in the deep water basin south of the Aleutian Islands. Ordination analysis of our sequences revealed nearly identical community structures between our Shelikof Strait and the deep water basin sites. Operational taxonomic unit analysis revealed that water samples from the Bering Sea sites shared more OTUs with the Shelikof Strait site than with the sea ice sample, despite the existence of sea ice in the Bering Sea, reflecting known circulation patterns out of the Gulf of Alaska. Richness increased with increasing latitude and decreasing temperature, suggesting that the base of food webs is susceptible to temperature perturbations.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alverson AJ, Kolnick L (2005) Intragenomic nucleotide polymorphism among small subunit (18S) rDNA paralogs in the diatom genus Skeletonema (Bacillariophyta). J Phycol 41:1248–1257

    Article  CAS  Google Scholar 

  • An S, Couteau C, Luo F, Neveu J, DuBow MS (2013) Bacterial diversity of surface sand samples from the Gobi and Taklamaken Deserts. Microb Ecol 66:850–860

    Article  PubMed  Google Scholar 

  • Aydin K, Mueter FJ (2007) The Bering Sea—a dynamic food web perspective. Deep Sea Res II 54:2501–2525

    Article  Google Scholar 

  • Bachy C, Dolan JR, López-Garcia P, Deschamps P, Moreira D (2013) Accuracy of protist diversity assessments: morphology compared with cloning and direct pyrosequencing of 18S rRNA genes and ITS regions using the conspicuous tintinnid ciliates as a case study. ISME J 7:244–255

    Article  CAS  PubMed  Google Scholar 

  • Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, Keeling P, Rohwer FL (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13:1192–1204

    Article  CAS  PubMed  Google Scholar 

  • Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 6:a016147

    Article  PubMed  PubMed Central  Google Scholar 

  • Carmack E, Barber D, Christensen J, Macdonald R, Rudels B, Sakshaug E (2006) Climate variability and physical forcing of the food webs and the carbon budget on panarctic shelves. Prog Oceanogr 71:145–181

    Article  Google Scholar 

  • Comeau AM, Li WKW, Tremblay JÉ, Carmack EC, Lovejoy C (2011) Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. PLoS ONE. doi:10.1371/journal.pone.0027492

    PubMed  PubMed Central  Google Scholar 

  • Cox G, Weeks W (1983) Equations for determining the gas and brine volumes in sea ice samples. J Glaciol 29:306–316

  • Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37

    Article  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fossheim M, Primicerio R, Johannesen E, Ingvaldsen RB, Aschan MM, Dolgov AV (2015) Recent warming leads to a rapid borealization of fish communities in the Arctic. Nat Clim Change 5:673–677

    Article  Google Scholar 

  • Galand PE, Lovejoy C, Vincent WF (2006) Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat Microb Ecol 44:115–126

    Article  Google Scholar 

  • Galand PE, Lovejoy C, Pouliot J, Garneau MÉ, Vincent WF (2008) Microbial community diversity and heterotrophic production in a coastal Arctic ecosystem: a Stamukhi lake and its source waters. Limnol Oceanogr 53:813–823

    Article  Google Scholar 

  • Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci 106:22427–22432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gittel A, Bárta J, Kohoutová I, Mikutta R, Owens S, Gilbert J, Schnecker J, Wild B, Hannisdal B, Maerz J, Lashchinskiy N (2014) Distinct microbial communities associated with buried soils in the Siberian tundra. ISME J 8:841–853

    Article  CAS  PubMed  Google Scholar 

  • Gradinger R (2009) Sea-ice algae: Major contributors to primary production and algal biomass in the Chukchi and Beaufort Seas during May/June 2002. Deep Sea Res II 56:1201–1212

    Article  CAS  Google Scholar 

  • Gradinger R, Bluhm BA, Hopcroft RR, Gebruk AV, Kosobokova K, Sirenko B, Węsławski (2010) Marine life in the Arctic. In: McIntyre AD (ed) Life in the world’s oceans: diversity, distribution, and abundance. Wiley-Blackwell, West Sussex, pp 183–202

    Chapter  Google Scholar 

  • Grattepanche JD, Santoferrara LF, McManus GB, Katz LA (2014) Diversity of diversity: conceptual and methodological differences in biodiversity estimates of eukaryotic microbes as compared to bacteria. Trends Microbiol 22:432–437

    Article  CAS  PubMed  Google Scholar 

  • Hassett BT, Ducluzeau AL, Collins RE, Gradinger R (2017) Spatial distribution of aquatic marine fungi across the western Arctic and sub-Arctic. Environ Microbiol 19:475–484

  • Hassett BT, Gradinger R (2016) Chytrids dominate Arctic marine fungal communities. Environ Microbiol 18:2001–2009

    Article  CAS  PubMed  Google Scholar 

  • Hassett BT, López JA, Gradinger R (2015) Two new species of marine saprotrophic sphaeroformids in the Mesomycetozoea isolated from the Sub-Arctic Bering Sea. Protist 166:310–322

    Article  PubMed  Google Scholar 

  • Hodges LR, Bano N, Hollibaugh JT, Yager PL (2005) Illustrating the importance of particulate organic matter to pelagic microbial abundance and community structure—an Arctic case study. Aquat Microb Ecol 40:217–227

    Article  Google Scholar 

  • Holmes RM, McClelland JW, Peterson BJ, Tank SE, Bulygina E, Eglinton TI, Gordeev VV, Gurtovaya TY, Raymond PA, Repeta DJ, Staples R (2012) Seasonal and annual fluxes of nutrients and organic matter from large rivers to the Arctic Ocean and surrounding seas. Estuar Coast 35:369–382

    Article  CAS  Google Scholar 

  • Howell-Kübler AN, Lessard EJ, Napp JM (1996) Springtime microprotozoan abundance and biomass in the southeastern Bering Sea and Shelikof Strait, Alaska. J Plankton Res 18:731–745

    Article  Google Scholar 

  • Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV (2002) Selection in the evolution of gene duplications. Genome Biol. doi:10.1186/gb-2002-3-2-research0008

    PubMed  PubMed Central  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leu E, Mundy CJ, Assmy P, Campbell K, Gabrielsen TM, Gosselin M, Juul-Pedersen T, Gradinger R (2015) Arctic spring awakening—steering principles behind the phenology of vernal ice algae blooms. Prog Oceanogr 139:151–170

    Article  Google Scholar 

  • Lewitus AJ, Horner RA, Caron DA, Garcia-Mendoza E, Hickey BM, Hunter M, Huppert DD, Kudela RM, Langlois GW, Largier JL, Lessard EJ (2012) Harmful algal blooms along the North American west coast region: history, trends, causes and impacts. Harmful Algae 19:133–159

    Article  Google Scholar 

  • Lovejoy C, Massana R, Pedrós-Alió C (2006) Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Appl Environ Microbiol 72:3085–3095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathis JT, Cross JN, Bates NR (2011) Coupling primary production and terrestrial runoff to ocean acidification and carbonate mineral suppression in the eastern Bering Sea. J Geophys Res. doi:10.1029/2010JC006453

    Google Scholar 

  • Moniz BJM, Kaczmarska I (2010) Barcoding of diatoms: nuclear encoded ITS revisited. Protist 161:7–34

    Article  CAS  PubMed  Google Scholar 

  • Moran SB, Lomas MW, Kelly RP, Gradinger R, Iken K, Mathis JT (2012) Seasonal succession of net primary productivity, particulate organic carbon export, and autotrophic community composition in the eastern Bering Sea. Deep Sea Res II 65–70:84–97

    Article  Google Scholar 

  • Mueter FJ, Litzow MA (2008) Sea ice retreat alters the biogeography of the Bering Sea continental shelf. Ecol Appl 18:309–320

    Article  PubMed  Google Scholar 

  • Nelson RJ, Ashjian CJ, Bluhm BA, Conlan KE, Gradinger RR, Grebmeier JM, Hill VJ, Hopcroft RR, Hunt BP, Joo HM, Kirchman DL (2014) Biodiversity and biogeography of the lower trophic taxa of the Pacific Arctic Region: sensitivities to climate change. In: Grebmeier J, Maslowski W (eds) The Pacific Arctic region: ecosystem status and trends in a rapidly changing environment. Springer, Netherlands, pp 269–336

    Google Scholar 

  • Paulus BC, Kanowski J, Gadek PA, Hyde KD (2006) Diversity and distribution of saprobic microfungi in leaf litter of an Australian tropical rainforest. Mycol Res 110:1441–1454

    Article  PubMed  Google Scholar 

  • Piepenburg D, Archambault P, Ambrose WG, Blanchard AL, Bluhm BA, Carroll ML, Conlan KE, Cusson M, Feder HM, Grebmeier JM, Jewett SC (2011) Towards a pan-Arctic inventory of the species diversity of the macro- and megabenthic fauna of the Arctic shelf seas. Mar Biodivers 41:51–70

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596

    Article  Google Scholar 

  • Roy K, Jablonski D, Valentine JW, Rosenberg G (1998) Marine latitudinal diversity gradients: tests of causal hypotheses. Proc Natl Acad Sci 95:3699–3702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW (2009) Introducing Mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serno S, Winckler G, Anderson RF, Hayes CT, McGee D, Machalett B, Ren H, Straub SM, Gersonde R, Haug GH (2014) Eolian dust input to the Subarctic North Pacific. Earth Planet Sci Lett 387:252–263

    Article  CAS  Google Scholar 

  • Sherr EB, Sherr BF, Ross C (2013) Microzooplankton grazing impact in the Bering Sea during spring sea ice conditions. Deep Sea Res II 94:57–67

    Article  CAS  Google Scholar 

  • Sorokin YI, Sorokin PY, Mamaeva TI (1996) Density and distribution of bacterioplankton and planktonic ciliates in the Bering Sea and North Pacific. J Plankton Res 18:1–16

    Article  Google Scholar 

  • Stabeno PJ, Schumacher JD, Ohtani K (1999) The physical oceanography of the Bering Sea. In: Loughlin T, Ohtani K (eds) Dynamics of the Bering Sea. University of Alaska Sea Grant, Fairbanks, pp 1–28

    Google Scholar 

  • Stabeno PJ, Bond NA, Kachel NB, Salo SA, Schumacher JD (2001) On the temporal variability of the physical environment over the south-eastern Bering Sea. Fish Oceanogr 10:81–98

    Article  Google Scholar 

  • Steele M, Ermold W, Zhang J (2008) Arctic Ocean surface warming trends over the past 100 years. Geophys Res Lett. doi:10.1029/2007GL031651

    Google Scholar 

  • Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19:21–31

    Article  CAS  PubMed  Google Scholar 

  • Suttle CA (2007) Marine viruses—major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  PubMed  Google Scholar 

  • Szymanski A, Gradinger R (2016) The diversity, abundance and fate of ice algae and phytoplankton in the Bering Sea. Polar Biol 39:309–325

    Article  Google Scholar 

  • Tsunogai S, Kusakabe M, Iizumi H, Koike I, Hattori A (1979) Hydrographic features of the deep water of the Bering Sea—the Sea of Silica. Deep Sea Res 26:641–659

    Article  CAS  Google Scholar 

  • Whitledge TE, Luchin VA (1999) Summary of chemical distributions and dynamics in the Bering Sea. In: Loughlin T, Ohtani K (eds) Dynamics of the Bering Sea. University of Alaska Sea Grant, Fairbanks, pp 217–249

    Google Scholar 

  • Yasuhara M, Hunt G, van Dijken G, Arrigo KR, Cronin TM, Wollenburg JE (2012) Patterns and controlling factors of species diversity in the Arctic Ocean. J Biogeogr 39:2081–2088.

    Article  Google Scholar 

Download references

Acknowledgements

This material is supported by National Science Foundation Award DGE-0801720, the Marine Ecosystem Sustainability in the Arctic and Subarctic (MESAS) IGERT #1303901. Sequence data have been deposited in the NCBI Sequence Read Archive under BioProject accession 305168. The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. T. Hassett.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Sampling rarefaction curves. Curves were generated after sequence vetting, subsampling (62,588) and clustering at 97% similarity (TIFF 164 kb)

Online Resource 2

Condensed taxonomy list of detected organisms in the Bering Sea and surrounding areas. Organisms classified to the taxonomic genus level are represented below. Select taxonomic clades in the Phaeophytes and fungi were represented by only sequences classifiable to Order and were included in this table. The majority of our sequences did not classify to the genus level and are not represented in this table. For example, the Prasinophytes were detected at every station, but Prasinoderma sp. is represented at only three stations (DOCX 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassett, B.T., Gradinger, R. Eukaryotic microbial richness increases with latitude and decreasing temperature in the Pacific Subarctic domain in late winter. Polar Biol 40, 2161–2169 (2017). https://doi.org/10.1007/s00300-017-2131-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-017-2131-2

Keywords

Navigation