Article | Published:

A globally distributed Syndiniales parasite dominates the Southern Ocean micro-eukaryote community near the sea-ice edge

The ISME Journalvolume 13pages734737 (2019) | Download Citation

Abstract

Syndiniales (Dinophyceae, Alveolata) are a diverse parasitic group common in all marine environments, but their ecological role remains poorly understood. Here we show an unprecedented dominance of a single Syndiniales group I operational taxonomic unit (OTU) across 3000 km of Southern Ocean transects near the sea-ice edge. This super-abundant OTU consistently represented >20%, and in some locations >50%, of eukaryote 18S rDNA sequences. Identical 18S V4 sequences have been isolated from seven Northern Hemisphere locations, and the OTU’s putative V9 rDNA sequence was detected at every station of the global Tara Oceans voyage. Although Syndiniales taxa display some host specificity, our identification of candidate Southern Ocean hosts suggests this OTU associates with distinct phyla in different parts of the world. Our results indicate Syndiniales are key players in surface waters near the vast and dynamic sea-ice edge in the world’s most biologically productive ocean.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    de Vargas C, Audic S, Henry N, Decelle J, Mahé F, Logares R, et al. Eukaryotic plankton diversity in the sunlit ocean. Science. 2015;348:1261605.

  2. 2.

    Pernice MC, Giner CR, Logares R, Perera-Bel J, Acinas SG, Duarte CM, et al. Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans. ISME J. 2016;10:945–58.

  3. 3.

    Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, et al. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol. 2008;10:3349–65.

  4. 4.

    Coats DW, Park MG. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): Parasite survival, infectivity, generation time, and host specificity. J Phycol. 2002;38:520–8.

  5. 5.

    Chambouvet A, Morin P, Marie D, Guillou L. Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science. 2008;322:1254–7.

  6. 6.

    Cleary AC, Durbin EG. Unexpected prevalence of parasite 18S rDNA sequences in winter among Antarctic marine protists. J Plankton Res. 2016;38:401–17.

  7. 7.

    Salomon PS, Granéli E. Neves MHCB, Rodriguez EG. Infection by Amoebophrya spp. parasitoids of dinoflagellates in a tropical marine coastal area. Aquat Microb Ecol. 2009;55:143–53.

  8. 8.

    Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J. 2015;9:968–79.

  9. 9.

    Bråte J, Krabberød AK, Dolven JK, Ose RF, Kristensen T, Bjørklund KR, et al. Radiolaria associated with large diversity of marine alveolates. Protist. 2012;163:767–77.

  10. 10.

    Thaler M, Lovejoy C. Distribution and diversity of a protist predator Cryothecomonas (Cercozoa) in Arctic marine waters. J Eukaryot Microbiol. 2012;59:291–9.

  11. 11.

    Bachy C, Lopez-Garcia P, Vereshchaka A, Moreira D. Diversity and vertical distribution of microbial eukaryotes in the snow, sea ice and seawater near the north pole at the end of the polar night. Front Microbiol. 2011;2:106.

  12. 12.

    Dolven JK, Lindqvist C, Albert VA, Bjørklund KR, Yuasa T, Takahashi O, et al. Molecular diversity of alveolates associated with neritic North Atlantic radiolarians. Protist. 2007;158:65–76.

  13. 13.

    Berdjeb L, Parada A, Needham DM, Fuhrman JA. Short-term dynamics and interactions of marine protist communities during the spring-summer transition. ISME J. 2018: e-pub ahead of print 2018; https://doi.org/10.1038/s41396-018-0097-x.

  14. 14.

    Yih W, Coats DW. Infection of Gymnodinium sanguineum by the dinoflagellate Amoebophrya sp.: effect of nutrient environment on parasite generation time, reproduction, and infectivity. J Eukaryot Microbiol. 2000;47:504–10.

  15. 15.

    Worden AZ, Follows MJ, Giovannoni SJ, Wilken S, Zimmerman AE, Keeling PJ. Environmental science. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science. 2015;347:1257594.

  16. 16.

    Warren CP, Pascual M, Lafferty KD, Kuris AM. The inverse niche model for food webs with parasites. Theor Ecol. 2010;3:285–94.

  17. 17.

    Frainer A, McKie BG, Amundsen PA, Knudsen R, Lafferty KD. Parasitism and the biodiversity-functioning relationship. Trends Ecol Evol. 2018;33:260–8.

  18. 18.

    Arrigo KR, van Dijken GL, Bushinsky S. Primary production in the Southern Ocean, 1997–2006. J Geophys Res. 2008;113:C08004 https://doi.org/10.1029/2007JC004551

  19. 19.

    Westwood K, Pearce I. Chlorophyll K-axis voyage V3 2015/16. Australian Antarctic Data Centre 2018. https://doi.org/10.4225/15/5a94c701b98a8.

Download references

Acknowledgements

We thank the Australian Antarctic Division (AAD) Science Technical Support Team and Aurora Australis crew for making this work happen. Karen Westwood and Imojen Pearce (AAD) provided chlorophyll data. Ben Raymond and Mike Sumner (AAD) helped access and interpret sea-ice melt data. Ruth Eriksen (CSIRO), Andrea Polanowski, Andrew Davidson and Karen Westwood (AAD) provided assistance with lab work. Martin Ostrowski (Macquarie University) ran the OTU taxonomy assignment. Rowan Trebilco (ACE CRC) provided advice on analyses. Contribution to the Australian Antarctic Science Kerguelen Axis project (AAS-4344). Molecular work funded through the Australian Antarctic Science Program (AAS-4313) and a Bioplatforms Australia Industry Access Voucher. This work was supported by the Australian Government’s Business Cooperative Research Centres Programme through the Antarctic Climate and Ecosystems Cooperative Research Centre, and the Australia Research Council’s Special Research Initiative for Antarctic Gateway Partnership (Project ID SR140300001).

Author information

Affiliations

  1. Antarctic Climate and Ecosystems Cooperative Research Centre, University of Tasmania, Hobart, Tasmania, 7001, Australia

    • Laurence J. Clarke
  2. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, 7001, Australia

    • Sophie Bestley
  3. Commonwealth Scientific and Industrial Research Organisation, Oceans and Atmosphere, Hobart, Tasmania, 7004, Australia

    • Sophie Bestley
    •  & Andrew Bissett
  4. Commonwealth Scientific and Industrial Research Organisation, Environomics FSP, Hobart, Tasmania, 7004, Australia

    • Andrew Bissett
  5. Australian Antarctic Division, Channel Highway, Kingston, Tasmania, 7050, Australia

    • Bruce E. Deagle

Authors

  1. Search for Laurence J. Clarke in:

  2. Search for Sophie Bestley in:

  3. Search for Andrew Bissett in:

  4. Search for Bruce E. Deagle in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Laurence J. Clarke.

Electronic supplementary material

About this article

Publication history

Received

Revised

Accepted

Published

Issue Date

DOI

https://doi.org/10.1038/s41396-018-0306-7