Diversity and distribution of heterotrophic flagellates in seawater of the Powell Basin, Antarctic Peninsula

Zhiyi Chen; Jianfeng He; Shunan Cao; Zhibo Lu; Musheng Lan; Hongyuan Zheng; Guangfu Luo; Fang Zhang

doi:10.33265/polar.v40.5389

Zhiyi Chen College of Environmental Science and Engineering, Tongji University, Shanghai, China; and Key Laboratory for Polar Science of Natural Resources Ministry, Polar Research Institute of China, Shanghai, China
Jianfeng He College of Environmental Science and Engineering, Tongji University, Shanghai, China; and Key Laboratory for Polar Science of Natural Resources Ministry, Polar Research Institute of China, Shanghai, China
Shunan Cao Key Laboratory for Polar Science of Natural Resources Ministry, Polar Research Institute of China, Shanghai, China
Zhibo Lu College of Environmental Science and Engineering, Tongji University, Shanghai, China
Musheng Lan Key Laboratory for Polar Science of Natural Resources Ministry, Polar Research Institute of China, Shanghai, China
Hongyuan Zheng College of Environmental Science and Engineering, Tongji University, Shanghai, China
Guangfu Luo Key Laboratory for Polar Science of Natural Resources Ministry, Polar Research Institute of China, Shanghai, China
Fang Zhang Key Laboratory for Polar Science of Natural Resources Ministry, Polar Research Institute of China, Shanghai, China

DOI: https://doi.org/10.33265/polar.v40.5389

Keywords: Heterotrophic picoflagellates, heterotrophic nanoflagellates, biodiversity, community structure

Abstract

Heterotrophic flagellates are essential components of the marine microbial food web. However, how the changes in flagellate populations reflect environmental changes in marine ecosystems is still unclear, especially in polar regions. In this study, we used pyrosequencing to examine the community structure of heterotrophic flagellates (HFs) in the Powell Basin’s surface waters of the northern Antarctic Peninsula. OTUs (operational taxonomic units) of different taxa and the correlations between community structure and environmental factors were analysed. Eight taxa of HFs were selected for the principal analysis: Telonemia, Picozoa, Rhizaria, Amoebozoa, Apusomonas, Centrohelida, Choanomonada and marine stramenopiles (MASTs). The HFs were defined as heterotrophic picoflagellates (HPFs; <3 μm) and heterotrophic nanoflagellates (HNFs; >3 μm, <20 μm), which had similar dominant phyla (MASTs and Telonemia). However, their taxonomic composition differed. Environmental factors exerted similar effects on the community structure of both HPFs and HNPs. Compared with the correlation between HPF and environmental factors, the correlation between HNF and environmental factors was stronger. Salinity, bacterial biomass and the biological interactions amongst dominant taxa were the main variables to influence the diversity and community structure of HFs.

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References

Ardyna M., Gosselin M., Michel C., Poulin M. & Tremblay J.E. 2011. Environmental forcing of phytoplankton community structure and function in the Canadian High Arctic: contrasting oligotrophic and eutrophic regions. Marine Ecology Progress Series 442, 37–57, doi: 10.3354/meps09378.

Arndt H., Dietrich D., Auer B., Cleven E.-J., Grafenhan T., Weitere M. & Mylnikov A.P. 2000. Functional diversity of heterotrophic flagellates in aquatic ecosystems. In B.S.C. Leadbeater & J.C. Green (eds.): The flagellates: unity, diversity and evolution. Pp. 240–268. London: Taylor & Francis.

Bonkowski M. 2004. Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 162, 617–631, doi: 10.1111/j.1469-8137.2004.01066.x.

Bråte J., Klaveness D., Rygh T., Jakobsen K.S. & Shalchian-Tabrizi K. 2010. Telonemia-specific environmental 18S rDNA PCR reveals unknown diversity and multiple marine–freshwater colonizations. BMC Microbiology 10, article no. 168, doi: 10.1186/1471-2180-10-168.

Cao S.N., He J.F., Zhang F., Lin L., Gao Y. & Zhou Q.M. 2019. Diversity and community structure of bacterioplankton in surface waters off the northern tip of the Antarctic Peninsula. Polar Research 38, article no. 3491, doi: 10.33265/polar.v38.3491.

Cermeno P. & Falkowski P.G. 2009. Controls on diatom biogeography in the ocean. Science 325, 1539–1541, doi: 10.1126/science.1174159.

Chen Z.Y., Lu Z.B., Gao Y., Hao Q. & He J.F. 2021. Determination of bacterioplankton abundance, production and carbon budget in the northwest Weddell Sea. Geomicrobiology Journal 38, 607–619, doi: 10.1080/01490451.2021.1914783.

Comeau A.M., Philippe B., Thaler M., Gosselin M., Poulin M. & Lovejoy C. 2013. Protists in Arctic drift and land-fast sea ice. Journal of Phycology 49, 229–240, doi: 10.1111/jpy.12026.

Dayel M.J., Alegado R.A., Fairclough S.R., Levin T.C., Nichols S.A., McDonald K. & King N. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Developmental Biology 357, 73–82, doi: 10.1016/j.ydbio.2011.06.003.

Domaizon I., Viboud S. & Fontvieille D. 2003. Taxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy—importance of mixotrophy. FEMS Microbiology Ecology 46, 317–329, doi: 10.1016/S0168-6496(03)00248-4.

Falk-Petersen S., Pavlov V., Timofeev S. & Sargent J.R. 2007. Climate variability and possible effects on Arctic food chains: the role of Calanus. In J.B. Ørbæk et al. (eds.): Arctic alpine ecosystems and people in a changing environment. Pp. 147–166. Berlin: Springer.

Fenchel T. & Finlay B.J. 2004. The ubiquity of small species: patterns of local and global diversity. Bioscience 54, 777–784, doi: 10.1641/0006-3568(2004)054[0777:Tuossp]2.0.Co;2.

Filker S., Stock A., Breiner H.W., Edgcomb V., Orsi W., Yakimov M.M. & Stoeck T. 2013. Environmental selection of protistan plankton communities in hypersaline anoxic deep-sea basins, eastern Mediterranean Sea. Microbiologyopen 2, 54–63, doi: 10.1002/mbo3.56.

Fortier L., Sirois P., Michaud J. & Barber D. 2006. Survival of Arctic cod larvae (Boreogadus saida) in relation to sea ice and temperature in the Northeast Water Polynya (Greenland Sea). Canadian Journal of Fisheries and Aquatic Sciences 63, 1608–1616, doi: 10.1139/F06-064.

Frias-Lopez J., Thompson A., Waldbauer J. & Chisholm S.W. 2009. Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters. Environmental Microbiology 11, 512–525, doi: 10.1111/j.1462-2920.2008.01793.x.

Garrison D.L., Gibson A., Coale S.L., Gowing M.M., Okolodkov Y.B., Fritsen C.H. & Jeffries M.O. 2005. Sea-ice microbial communities in the Ross Sea: Autumn and summer biota. Marine Ecology Progress Series 300, 39–52, doi: 10.3354/meps300039.

Grebert T., Dore H., Partensky F., Farrant G.K., Boss E.S., Picheral M., Guidi L., Pesant S., Scanlan D.J., Wincker P., Acinas S.G., Kehoe D.M. & Garczarek L. 2018. Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 115, E2010–E2019, doi: 10.1073/pnas.1717069115.

Hamilton A.K., Lovejoy C., Galand P.E. & Ingram R.G. 2008. Water masses and biogeography of picoeukaryote assemblages in a cold hydrographically complex system. Limnology and Oceanography 53, 922–935, doi: 10.4319/lo.2008.53.3.0922.

Hanson C.A., Fuhrman J.A., Horner-Devine M.C. & Martiny J.B. 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nature Reviews Microbiology 10, 497–506, doi: 10.1038/nrmicro2795.

He J.F., Zhang F., Lin L., Cai M.H., Yang H.Z. & Wang X.G. 2012. Effects of the 2010 Chile and 2011 Japan tsunamis on the Antarctic coastal waters as detected via online mooring system. Antarctic Science 24, 665–671, doi: 10.1017/S0954102012000326.

Hernandez-Molina F.J., Larter R.D., Rebesco M. & Maldonado A. 2006. Miocene reversal of bottom water flow along the Pacific Margin of the Antarctic Peninsula: stratigraphic evidence from a contourite sedimentary tail. Marine Geology 228, 93–116, doi: 10.1016/j.margeo.2005.12.010.

Ikavalko J. & Gradinger R. 1997. Flagellates and heliozoans in the Greenland Sea ice studied alive using light microscopy. Polar Biology 17, 473–481, doi: 10.1007/s003000050145.

Jiuxin S., Yongming S., Yutian J., Guanghua H. & Miao W. 2016. Water masses and exchanges in the region around the northern tip of the Antarctic Peninsula observed in summer 2011/2012. Chinese Journal of Polar Research 28, 67–79.

Jones S.E. & Lennon J.T. 2010. Dormancy contributes to the maintenance of microbial diversity. Proceedings of the National Academy of Sciences of the United States of America 107, 5881–5886, doi: 10.1073/pnas.0912765107.

Laidre K.L., Stirling I., Lowry L.F., Wiig O., Heide-Jorgensen M.P. & Ferguson S.H. 2008. Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat change. Ecological Applications 18, S97–S125, doi: 10.1890/06-0546.1.

Li W.K.W., McLaughlin F.A., Lovejoy C. & Carmack E.C. 2009. Smallest algae thrive as the Arctic Ocean freshens. Science 326, 539–539, doi: 10.1126/science.1179798.

Lin Y.C., Campbell T., Chung C.C., Gong G.C., Chiang K.P. & Worden A.Z. 2012. Distribution patterns and phylogeny of marine stramenopiles in the north Pacific Ocean. Applied and Environmental Microbiology 78, 3387–3399, doi: 10.1128/AEM.06952-11.

Logares R., Audic S., Santini S., Pernice M.C., de Vargas C. & Massana R. 2012. Diversity patterns and activity of uncultured marine heterotrophic flagellates unveiled with pyrosequencing. ISME Journal 6, 1823–1833, doi:10.1038/ismej.2012.36.

Lovejoy C., Massana R. & Pedros-Alio C. 2006. Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Applied Environmental Microbiology 72, 3085–3095, doi: 10.1128/AEM.72.5.3085-3095.2006.

Lovejoy C., Vincent W.F., Bonilla S., Roy S., Martineau M.J., Terrado R., Potvin M., Massana R. & Pedros-Alio C. 2007. Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. Journal of Phycology 43, 78–89, doi: 10.1111/j.1529-8817.2006.00310.x.

Luo W., Li H.R., Gao S.Q., Yu Y., Lin L. & Zeng Y.X. 2016. Molecular diversity of microbial eukaryotes in sea water from Fildes Peninsula, King George Island, Antarctica. Polar Biology 39, 605–616, doi: 10.1007/s00300-015-1815-8.

Massana R. 2011. Eukaryotic picoplankton in surface oceans. Annual Review of Microbiology 65, 91–110, doi: 10.1146/annurev-micro-090110-102903.

Massana R., Castresana J., Balague V., Guillou L., Romari K., Groisillier A., Valentin K. & Pedros-Alio C. 2004. Phylogenetic and ecological analysis of novel marine stramenopiles. Applied Environmental Microbiology 70, 3528–3534, doi: 10.1128/AEM.70.6.3528-3534.2004.

Massana R., Terrado R., Forn I., Lovejoy C. & Pedros-Alio C. 2006. Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environmental Microbiology 8, 1515–1522, doi: 10.1111/j.1462-2920.2006.01042.x.

Massana R., Unrein F., Rodriguez-Martinez R., Forn I., Lefort T., Pinhassi J. & Not F. 2009. Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME Journal 3, 588–596, doi: 10.1038/ismej.2008.130.

McKenna S., Meyer M., Gregg C. & Gerber S. 2016. s-CorrPlot: an interactive scatterplot for exploring correlation. Journal of Computational and Graphical Statistics 25, 445–463, doi: 10.1080/10618600.2015.1021926.

Monier A., Sudek S., Fast N.M. & Worden A.Z. 2013. Gene invasion in distant eukaryotic lineages: discovery of mutually exclusive genetic elements reveals marine biodiversity. ISME Journal 7, 1764–1774, doi: 10.1038/ismej.2013.70.

Müller T.J. 2007. Determination of salinity. In K. Grasshoff et al. (eds.): Methods of seawater analysis. 3rd edn. Pp. 41–74. Weinheim: Wiley-VCH.

Mylnikova Z.M. & Mylnikov A.P. 2012. Structure of filose amoeba Rhogostoma minus Belar 1921 (Cryomonadida, Cercozoa) cell. Inland Water Biology 5, 236–240, doi: 10.1134/S1995082912020101.

Orsi W., Edgcomb V., Jeon S., Leslin C., Bunge J., Taylor G.T., Varela R. & Epstein S. 2011. Protistan microbial observatory in the Cariaco Basin, Caribbean. II. Habitat specialization. ISME Journal 5, 1357–1373, doi: 10.1038/ismej.2011.7.

Piwosz K. & Pernthaler J. 2010. Seasonal population dynamics and trophic role of planktonic nanoflagellates in coastal surface waters of the southern Baltic Sea. Environmental Microbiology 12, 364–377, doi: 10.1111/j.1462-2920.2009.02074.x.

Piwosz K., Wiktor J.M., Niemi A., Tatarek A. & Michel C. 2013. Mesoscale distribution and functional diversity of picoeukaryotes in the first-year sea ice of the Canadian Arctic. ISME Journal 7, 1461–1471, doi:10.1038/ismej.2013.39.

Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J. & Glockner F.O. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research 35, 7188–7196, doi: 10.1093/nar/gkm864.

Rodriguez-Martinez R., Rocap G., Salazar G. & Massana R. 2013. Biogeography of the uncultured marine picoeukaryote MAST-4: temperature-driven distribution patterns. ISME Journal 7, 1531–1543, doi: 10.1038/ismej.2013.53.

Schlitzer R., Anderson R.F., Dodas E.M., Lohan M., Geibere W., Tagliabue A., Bowie A., Jeandel C., Maldonado M.T., Landing W.M., Cockwell D., Abadie C., Abouchami W., Achterberg E.P., Agather A., Aguliar-Islas A., van Aken H.M., Andersen M., Archer C., Auro M., de Baar H.J., Baars O., Baker A.R., Bakker K., Basak C., Baskaran M., Bates N.R., Bauch D., van Beek P., et al. 2018. The GEOTRACES Intermediate Data Product 2017. Chemical Geology 493, 210–223, doi: 10.1016/j.chemgeo.2018.05.040.

Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J. & Weber C.F. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied Environmental Microbiology 75, 7537–7541, doi: 10.1128/AEM.01541-09.

Seenivasan R., Sausen N., Medlin L.K. & Melkonian M. 2013. Picomonas judraskeda gen. et sp nov.: the first identified member of the Picozoa phylum nov., a widespread group of picoeukaryotes, formerly known as “picobiliphytes.” PLoS One 8, article no. e59565, doi: 10.1371/journal.pone.0059565.

Sherr E.B. & Sherr B.F. 2002. Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81, 293–308, doi: 10.1023/a:1020591307260.

Sohrin R., Imazawa M., Fukuda H. & Suzuki Y. 2010. Full-depth profiles of prokaryotes, heterotrophic nanoflagellates, and ciliates along a transect from the equatorial to the Subarctic central Pacific Ocean. Deep-Sea Research Part II 57, 15371–15350, doi: 10.1016/j.dsr2.2010.02.020.

Thaler M. & Lovejoy C. 2012. Distribution and diversity of a protist predator Cryothecomonas (Cercozoa) in Arctic marine waters. Journal of Eukaryotic Microbiology 59, 291–299, doi: 10.1111/j.1550-7408.2012.00631.x.

Thaler M. & Lovejoy C. 2015. Biogeography of heterotrophic flagellate populations indicates the presence of generalist and specialist taxa in the Arctic Ocean. Applied Environmental Microbiology 81, 2137–2148, doi: 10.1128/AEM.02737-14.

Waleron M., Waleron K., Vincent W.F. & Wilmotte A. 2007. Allochthonous inputs of riverine picocyanobacteria to coastal waters in the Arctic Ocean. FEMS Microbiology Ecology 59, 356–365, doi: 10.1111/j.1574-6941.2006.00236.x.

Zhang F., Cao S.A., Gao Y. & He J.F. 2019. Distribution and environmental correlations of picoeukaryotes in an Arctic fjord (Kongsfjorden, Svalbard) during the summer. Polar Research 38, article no. 3390, doi: 10.33265/polar.v38.3390.

Zhang F., He J.F., Lin L. & Jin H.Y. 2015. Dominance of picophytoplankton in the newly open surface water of the central Arctic Ocean. Polar Biology 38, 1081–1089, doi: 10.1007/s00300-015-1662-7.