Water masses shape pico-nano eukaryotic communities of the Weddell Sea
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36653511
PubMed Central
PMC9849203
DOI
10.1038/s42003-023-04452-7
PII: 10.1038/s42003-023-04452-7
Knihovny.cz E-zdroje
- MeSH
- ekosystém * MeSH
- Eukaryota * MeSH
- kyslík MeSH
- oceány a moře MeSH
- voda MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- oceány a moře MeSH
- Názvy látek
- kyslík MeSH
- voda MeSH
Polar oceans belong to the most productive and rapidly changing environments, yet our understanding of this fragile ecosystem remains limited. Here we present an analysis of a unique set of DNA metabarcoding samples from the western Weddell Sea sampled throughout the whole water column and across five water masses with different characteristics and different origin. We focus on factors affecting the distribution of planktonic pico-nano eukaryotes and observe an ecological succession of eukaryotic communities as the water masses move away from the surface and as oxygen becomes depleted with time. At the beginning of this succession, in the photic zone, algae, bacteriovores, and predators of small eukaryotes dominate the community, while another community develops as the water sinks deeper, mostly composed of parasitoids (syndinians), mesoplankton predators (radiolarians), and diplonemids. The strongly correlated distribution of syndinians and diplonemids along the depth and oxygen gradients suggests their close ecological link and moves us closer to understanding the biological role of the latter group in the ocean ecosystem.
Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic
Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic
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Guillou L, et al. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata) Environ. Microbiol. 2008;10:3349–3365. doi: 10.1111/j.1462-2920.2008.01731.x. PubMed DOI
Massana R. Eukaryotic picoplankton in surface oceans. Annu. Rev. Microbiol. 2011;65:91–110. doi: 10.1146/annurev-micro-090110-102903. PubMed DOI
Rocke E, Pachiadaki MG, Cobban A, Kujawinski EB, Edgcomb VP. Protist community grazing on prokaryotic prey in deep ocean water masses. PLoS ONE. 2015;10:e0124505. doi: 10.1371/journal.pone.0124505. PubMed DOI PMC
de Vargas C, et al. Eukaryotic plankton diversity in the sunlit ocean. Science. 2015;348:1261605. doi: 10.1126/science.1261605. PubMed DOI
Ibarbalz FM, et al. Global trends in marine plankton diversity across kingdoms of life. Cell. 2019;179:1084–1097. doi: 10.1016/j.cell.2019.10.008. PubMed DOI PMC
Cordier, T. et al. Patterns of eukaryotic diversity from the surface to the deep-ocean sediment. Sci. Adv.8, 10.1126/sciadv.abj9309 (2022). PubMed PMC
Giner CR, et al. Marked changes in diversity and relative activity of picoeukaryotes with depth in the world ocean. ISME J. 2020;14:437–449. doi: 10.1038/s41396-019-0506-9. PubMed DOI PMC
Obiol A, et al. A metagenomic assessment of microbial eukaryotic diversity in the global ocean. Mol. Ecol. Resour. 2020;20:718–731. doi: 10.1111/1755-0998.13147. PubMed DOI
Pernice MC, et al. Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans. ISME J. 2016;10:945–958. doi: 10.1038/ismej.2015.170. PubMed DOI PMC
Santoferrara L, et al. Perspectives from ten years of protist studies by high‐throughput metabarcoding. J. Eukaryot. Microbiol. 2020;67:612–622. doi: 10.1111/jeu.12813. PubMed DOI
Schoenle A, et al. High and specific diversity of protists in the deep-sea basins dominated by diplonemids, kinetoplastids, ciliates and foraminiferans. Commun. Biol. 2021;4:1–10. doi: 10.1038/s42003-021-02012-5. PubMed DOI PMC
Sommeria-Klein G, et al. Global drivers of eukaryotic plankton biogeography in the sunlit ocean. Science. 2021;374:594–599. doi: 10.1126/science.abb3717. PubMed DOI
Tremblay JÉ, et al. Global and regional drivers of nutrient supply, primary production and CO2 drawdown in the changing Arctic Ocean. Prog. Oceanogr. 2015;139:171–196. doi: 10.1016/j.pocean.2015.08.009. DOI
Zoccarato L, Pallavicini A, Cerino F, Umani SF, Celussi M. Water mass dynamics shape Ross Sea protist communities in mesopelagic and bathypelagic layers. Prog. Oceanogr. 2016;149:16–26. doi: 10.1016/j.pocean.2016.10.003. DOI
Biggs TEG, Huisman J, Brussaard CPD. Viral lysis modifies seasonal phytoplankton dynamics and carbon flow in the Southern Ocean. ISME J. 2021;15:3615–3622. doi: 10.1038/s41396-021-01033-6. PubMed DOI PMC
Clarke LJ, Bestley S, Bissett A, Deagle BE. A globally distributed Syndiniales parasite dominates the Southern Ocean micro-eukaryote community near the sea-ice edge. ISME J. 2019;13:734–737. doi: 10.1038/s41396-018-0306-7. PubMed DOI PMC
Gast RJ, Fay SA, Sanders RW. Mixotrophic activity and diversity of Antarctic marine protists in austral summer. Front. Mar. Sci. 2018;5:13. doi: 10.3389/fmars.2018.00013. DOI
Grattepanche JD, Jeffrey WH, Gast RJ, Sanders RW. Diversity of microbial eukaryotes along the West Antarctic Peninsula in austral spring. Front. Microbiol. 2022;13:844856. doi: 10.3389/fmicb.2022.844856. PubMed DOI PMC
Hamilton M, et al. Spatiotemporal variations in Antarctic protistan communities highlight phytoplankton diversity and seasonal dominance by a novel cryptophyte lineage. mBio. 2021;12:e0297321. doi: 10.1128/mBio.02973-21. PubMed DOI PMC
Lin Y, et al. Decline in plankton diversity and carbon flux with reduced sea ice extent along the Western Antarctic Peninsula. Nat. Commun. 2021;12:4948. doi: 10.1038/s41467-021-25235-w. PubMed DOI PMC
Martin K, et al. The biogeographic differentiation of algal microbiomes in the upper ocean from pole to pole. Nat. Commun. 2021;12:5483. doi: 10.1038/s41467-021-25646-9. PubMed DOI PMC
Vernet M, et al. The Weddell Gyre, Southern Ocean: present knowledge and future challenges. Rev. Geophysics. 2019;57:623–708. doi: 10.1029/2018RG000604. DOI
Callahan JE. The structure and circulation of deep water in the Antarctic. Deep‐Sea Res. 1972;19:563–575.
Janout MA, et al. FRIS revisited in 2018: on the circulation and water masses at the Filchner and Ronne ice shelves in the southern Weddell Sea. J. Geophys. Res.: Oceans. 2021;126:e2021JC017269. doi: 10.1029/2021JC017269. DOI
Orsi AH, Smethie WM, Bullister JL. On the total input of Antarctic waters to the deep ocean: a preliminary estimate from chlorofluorocarbon measurements. J. Geophys. Res. 2002;107:3122. doi: 10.1029/2001JC000976. DOI
Hoppema M, Fahrbach E, Schröder M. On the total carbon dioxide and oxygen signature of the circumpolar deep water in the Weddell Gyre. Oceanol. Acta. 1997;20:783–798.
Karstensen J, Tomczak M. Age determination of mixed water masses using CFC and oxygen data. J. Geophys. Res. 1998;103:18599–18609. doi: 10.1029/98JC00889. DOI
De Cáceres M, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90:3566–3574. doi: 10.1890/08-1823.1. PubMed DOI
De Cáceres M, Legendre P, Moretti M. Improving indicator species analysis by combining groups of sites. Oikos. 2010;119:1674–1684. doi: 10.1111/j.1600-0706.2010.18334.x. DOI
Dufrene M, Legendre P. Species assemblages and indicator species: the need for a flexible asymetrical approach. Ecol. Monogr. 1997;67:345–366.
Agogué H, Lamy D, Neal PR, Sogin ML, Herndl GJ. Water mass-specificity of bacterial communities in the North Atlantic revealed by massively parallel sequencing. Mol. Ecol. 2011;20:258–274. doi: 10.1111/j.1365-294X.2010.04932.x. PubMed DOI PMC
Celussi M, Bergamasco A, Cataletto B, Umani SF, Del Negro P. Water masses bacterial community structure and microbial activities in the Ross Sea, Antarctica. Antarct. Sci. 2010;22:361–370. doi: 10.1017/S0954102010000192. DOI
Galand PE, Potvin M, Casamayor EO, Lovejoy C. Hydrography shapes bacterial biogeography of the deep Arctic Ocean. ISME J. 2010;4:564–576. doi: 10.1038/ismej.2009.134. PubMed DOI
Hamdan LJ. Ocean currents shape the microbiome of Arctic marine sediments. ISME J. 2013;7:685–696. doi: 10.1038/ismej.2012.143. PubMed DOI PMC
Wilkins D, van Sebille E, Rintoul SR, Lauro FM, Cavicchioli R. Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nat. Commun. 2013;4:2457. doi: 10.1038/ncomms3457. PubMed DOI
Flegontova O, et al. Extreme diversity of diplonemid eukaryotes in the ocean. Curr. Biol. 2016;26:3060–3065. doi: 10.1016/j.cub.2016.09.031. PubMed DOI
Barnes MA, et al. Environmental conditions influence eDNA persistence in aquatic systems. Environ. Sci. Technol. 2014;48:1819–1827. doi: 10.1021/es404734p. PubMed DOI
Jeong HJ, et al. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. 2010;45:65–91. doi: 10.1007/s12601-010-0007-2. DOI
Stoecker DK, Hansen PJ, Caron DA, Mitra A. Mixotrophy in the marine Plankton. Ann. Rev. Mar. Sci. 2016;9:311–335. doi: 10.1146/annurev-marine-010816-060617. PubMed DOI
Boeuf D, et al. Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean. Proc. Natl Acad. Sci. USA. 2019;116:11824–11832. doi: 10.1073/pnas.1903080116. PubMed DOI PMC
Gutierrez-Rodriguez A, et al. High contribution of Rhizaria (Radiolaria) to vertical export in the California Current Ecosystem revealed by DNA metabarcoding. ISME J. 2019;13:964–976. doi: 10.1038/s41396-018-0322-7. PubMed DOI PMC
Lampitt RS, Salter I, Johns D. Radiolaria: major exporters of organic carbon to the deep ocean. Glob. Biogeochem. Cycles. 2009;23:GB1010. doi: 10.1029/2008GB003221. DOI
Suzuki, N. & Not, F. In Marine Protists: Diversity and Dynamics 179–222 (Springer Japan, 2015).
Decelle J, et al. Diversity, ecology and biogeochemistry of cyst-forming Acantharia (Radiolaria) in the oceans. PLoS ONE. 2013;8:e53598. doi: 10.1371/journal.pone.0053598. PubMed DOI PMC
Tashyreva D, et al. Diplonemids—a review on “new“ flagellates on the oceanic block. Protist. 2022;173:125868. doi: 10.1016/j.protis.2022.125868. PubMed DOI
Flegontova O, et al. Environmental determinants of the distribution of planktonic diplonemids and kinetoplastids in the oceans. Environ. Microbiol. 2020;22:4014–4031. doi: 10.1111/1462-2920.15190. PubMed DOI
Xu D, et al. Microbial eukaryote diversity and activity in the water column of the South China sea based on DNA and RNA high throughput sequencing. Front. Microbiol. 2017;8:1121. doi: 10.3389/fmicb.2017.01121. PubMed DOI PMC
Bråte J, et al. Radiolaria associated with large diversity of marine alveolates. Protist. 2012;163:767–777. doi: 10.1016/j.protis.2012.04.004. PubMed DOI
Strassert JFH, et al. Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates. ISME J. 2017;12:304–308. doi: 10.1038/ismej.2017.167. PubMed DOI PMC
Yabuki A, Tame A. Phylogeny and reclassification of Hemistasia phaeocysticola (Scherffel) Elbrächter & Schnepf, 1996. J. Eukaryot. Microbiol. 2015;62:426–429. doi: 10.1111/jeu.12191. PubMed DOI
Larsen J, Patterson J. Some flagellates (Protista) from tropical marine sediments. J. Nat. Hist. 1990;24:801–937. doi: 10.1080/00222939000770571. DOI
Prokopchuk G, et al. Trophic flexibility of marine diplonemids - switching from osmotrophy to bacterivory. ISME J. 2022;16:1409–1419. doi: 10.1038/s41396-022-01192-0. PubMed DOI PMC
Arístegui J, Gasol J. Microbial oceanography of the dark ocean’s pelagic realm. Limnol. Oceanogr. 2009;54:1501–1529. doi: 10.4319/lo.2009.54.5.1501. DOI
Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE. 2009;4:e6372. doi: 10.1371/journal.pone.0006372. PubMed DOI PMC
Mahé F, Rognes T, Quince C, de Vargas C, Dunthorn M. Swarm v2: highly-scalable and high-resolution amplicon clustering. PeerJ. 2015;3:e1420. doi: 10.7717/peerj.1420. PubMed DOI PMC
Kolisko M, et al. EukRef-excavates: seven curated SSU ribosomal RNA gene databases. Database. 2020;2020:baaa080. PubMed PMC
Adl SM, et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 2019;66:4–119. doi: 10.1111/jeu.12691. PubMed DOI PMC
Salazar G, et al. Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell. 2019;179:1068–1083. doi: 10.1016/j.cell.2019.10.014. PubMed DOI PMC