Abstract
Passive sinking of particulate organic matter (POM) is the main mechanism through which the biological pump transports surface primary production to the ocean interior. However, the contribution and variability of different biological sources to vertical export is not fully understood. Here, we use DNA metabarcoding of the 18S rRNA gene and particle interceptor traps (PITs) to characterize the taxonomic composition of particles sinking out of the photic layer in the California Current Ecosystem (CCE), a productive system with high export potential. The PITs included formalin-fixed and ‘live’ traps to investigate eukaryotic communities involved in the export and remineralization of sinking particles. Sequences affiliated with Radiolaria dominated the eukaryotic assemblage in fixed traps (90%), with Dinophyta and Metazoa making minor contributions. The prominence of Radiolaria decreased drastically in live traps, possibly due to selective consumption by copepods, heterotrophic nanoflagellates, and phaeodarians that were heavily enriched in these traps. These patterns were consistent across the water masses surveyed extending from the coast to offshore, despite major differences in productivity and trophic structure of the epipelagic plankton community. Our findings identify Radiolaria as major actors in export fluxes in the CCE.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Turner JT. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr. 2015;130:205–48.
Eppley RW, Peterson BJ. Particulate organic -matter flux and planktonic new production in the deep ocean. Nature. 1979;282:677–80.
Henson SA, Sanders R, Madsen E, Morris PJ, Le Moigne F, Quartly GD. A reduced estimate of the strength of the ocean’s biological carbon pump. Geophys Res Lett. 2011;38:1–5.
Laws EA, Falkowski PG, Smith WO, Ducklow H, McCarthy JJ. Temperature effects on export production in the open ocean. Glob Biogeochem Cycles. 2000;14:1231–46.
Boyd PW, Newton PP. Does planktonic community structure determine downward particulate organic carbon flux in different oceanic provinces? Deep Sea Res Part I-Oceanogr Res Pap. 1999;46:63–91.
Guidi L, Stemmann L, Jackson GA. Effects of phytoplankton community on production, size and export of large aggregates: A world-ocean analysis. Limnol Oceanogr. 2009;54:1951–63.
Stukel MR, Landry MR, Benitez-Nelson CR, Goericke R. Trophic cycling and carbon export relationships in the California Current Ecosystem. Limnol Oceanogr. 2011;56:1866–78.
Giering SLC, Sanders R, Lampitt RS, Anderson TR, Tamburini C, Boutrif M, et al. Reconciliation of the carbon budget in the ocean’s twilight zone. Nature. 2014;507:480–517.
Lampitt RS, Noji T, Vonbodungen B. What happens to zooplankton fecal pellets - implications for material flux. Mar Biol. 1990;104:15–23.
Steinberg DK, Van Mooy BAS, Buesseler KO, Boyd PW, Kobari T, Karl DM. Bacterial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone. Limnol Oceanogr. 2008;53:1327–38.
Steinberg DK, Landry MR. Zooplankton and the Ocean Carbon Cycle. Ann Rev Mar Sci. 2017;9:413–44.
Caron DA, Davis PG, Madin LP, Sieburth JM. Enrichment of microbial- populations in macroaggregates (marine snow) from surface waters of the North- Atlantic. J Mar Res. 1986;44:543–65.
Alldredge AL, Silver MW. Characteristics, dynamics and significance of marine snow. Prog Oceanogr. 1988;20:41–82.
Agusti S, González-Gordillo JI, Vaqué D, Estrada M, Cerezo MI, Salazar G, et al. Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump. Nat Commun. 2015;6:7608.
Martin P, Lampitt RS, Perry MJ, Sanders R, Lee C, D’Asaro E. Export and mesopelagic particle flux during a North Atlantic spring diatom bloom. Deep Sea Res Part I-Oceanogr Res Pap. 2011;58:338–49.
Smetacek V, Klaas C, Strass VH, Assmy P, Montresor M, Cisewski B, et al. Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature. 2012;487:313–9.
Knauer GA, Martin JH, Bruland KW. Fluxes of particulate carbon, nitrogen, and phosphorus in the upper water column of the Northeast Pacific. Deep Sea Res. 1979;26:97–108.
Burd AB, Hansell DA, Steinberg DK, Anderson TR, Aristegui J, Baltar F, et al. Assessing the apparent imbalance between geochemical and biochemical indicators of meso- and bathypelagic biological activity: What the @$#! is wrong with present calculations of carbon budgets? Deep Sea Res Part II-Top Stud Oceanogr. 2010;57:1557. 1571
Herndl GJ, Reinthaler T. Microbial control of the dark end of the biological pump. Nat Geosci. 2013;6:718–24.
Bochdansky AB, Jericho MH, Herndl GJ. Development and deployment of a point-source digital inline holographic microscope for the study of plankton and particles to a depth of 6000 m. Limnol Oceanogr. 2013;11:28–40.
Amacher J, Neuer S, Anderson I, Massana R. Molecular approach to determine contributions of the protist community to particle flux. Deep Sea Res Part I Oceanogr Res Pap. 2009;56:2206–15.
Fontanez KM, Eppley JM, Samo TJ, Karl DM, DeLong EF. Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre. Front Microbiol. 2015;6:1–14.
Ohman M, Barbeau K, Franks P, Goericke R, Landry M, Miller A. Ecological Transitions in a Coastal Upwelling Ecosystem. Oceanography. 2013;26:210–9.
Taylor AG, Landry MR, Selph KE, Wokuluk JJ. Temporal and spatial patterns of microbial community biomass and composition in the Southern California Current Ecosystem. Deep Sea Res Part II Top Stud Oceanogr. 2015;112:117–28.
Landry MR, Ohman MD, Goericke R, Stukel MR, Tsyrklevich K. Lagrangian studies of phytoplankton growth and grazing relationships in a coastal upwelling ecosystem off Southern California. Prog Oceanogr. 2009;83:208–16.
Stukel MR, Aluwihare LI, Barbeau KA, Chekalyuk AM, Goericke R, Miller AJ, et al. Mesoscale ocean fronts enhance carbon export due to gravitational sinking and subduction. Proc Natl Acad Sci USA. 2017;114:1252–7.
Knauer GA, Karl DM, Martin JH, Hunter CN. In situ effects of selected preservatives on total carbon, nitrogen and metals collected in sediment traps. J Mar Res. 1984;42:445–62.
Karl DM, Knauer GA. Detritus-microbe interactions in the marine pelagic environment - selected results from the VERTEX experiment. Bull Mar Sci. 1984;35:550–6.
Lee C, Hedges JI, Wakeham SG, Zhu N. Effectiveness of various treatments in retarding microbial activity in sediment trap material and their effects on the collection of swimmers. Limnol Oceanogr. 1992;37:117–30.
Beers JR, Stewart GL. Preservation of acantharians in fixed plankton samples. Limnol Oceanogr. 1970;15:825–7.
Stukel MR, Ohman MD, Benitez-Nelson CR, Landry MR. Contributions of mesozooplankton to vertical carbon export in a coastal upwelling system. Mar Ecol Prog Ser. 2013;491:47–65.
Stukel MR, Kahru M, Benitez‐Nelson CR, Décima M, Goericke R, Landry MR, et al. Using Lagrangian‐based process studies to test satellite algorithms of vertical carbon flux in the eastern North Pacific Ocean. J Geophys Res Ocean. 2015;120:7208–22.
Amacher J, Neuer S, Lomas M. DNA-based molecular fingerprinting of eukaryotic protists and cyanobacteria contributing to sinking particle flux at the Bermuda Atlantic time-series study. Deep Sea Res Part II Top Stud Oceanogr. 2013;93:71–472.
Gordon LI, Jennings JC, Ross AA, and Krest JM. A suggested protocol for continuous flow automated analysis of seawater nutrients in the WOCE hydrographic program and the Joint Global Ocean Fluxes Study. Grp Tech Rpt 92-1, OSU Coll Oceanogr Descr Chem Oc. 1992.
Michaels AF, Caron DA, Swanberg NR, Howse FA, Michaels CM. Planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda: abundance, biomass and vertical flux. J Plankton Res. 1995;17:131–63.
Piredda R, Tomasino MP, D’Erchia AM, Manzari C, Pesole G, Montresor M, et al. Diversity and temporal patterns of planktonic protist assemblages at a Mediterranean Long Term Ecological Research site. FEMS Microbiol Ecol. 2017;93. https://doi.org/10.1093/femsec/fiw200.
Goecks J, Nekrutenko A, Taylor J. Lessons learned from Galaxy, a web-based platform for high-throughput genomic analyses. 2012;1–6. https://doi.org/10.1109/eScience.2012.6404442.
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 Env Microbiol. 2009;75:7537–41.
Edgar R, Haas B, Clemente J, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.
Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub- unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013;41:D597–604.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: Community Ecology Package. R package version 2.4-5. 2017. https://CRAN.R-project.org/package=vegan.
Wickham H. ggplot2: Elegant Graphics for Data Analysis. NewYork: Springer-Verlag; 2009.
Tennekes M. Treemap: Treemap Visualization. R package version 2.4-2. 2017.
Hammer Ø, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. In: Harper DAT (ed). Palaeontol Electron 2001;4:1–9.
Lopes dos Santos A, Pollina T, Gourvil P, Corre E, Marie D, Garrido JL, et al. Chloropicophyceae, a new class of picophytoplanktonic prasinophytes. Sci Rep. 2017;7:14019.
Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ. Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol. 2007;9:1233–52.
Lin Y, Cassar N, Marchetti A, Moreno C, Ducklow H, Li Z. Specific eukaryotic plankton are good predictors of net community production in the Western Antarctic Peninsula. Sci Rep. 2017;7:14845.
de Vargas C, Audic S, Henry N, Decelle J, Mahe F, Logares R, et al. Eukaryotic plankton diversity in the sunlit ocean. Science 2015; 348:1261605.
Pearman JK, Casas L, Merle T, Michell C, Irigoien X. Bacterial and protist community changes during a phytoplankton bloom. Limnol Oceanogr. 2016;61:198–213.
Lopes dos Santos A, Gourvil P, Tragin M, Noel MH, Decelle J, Romac S, et al. Diversity and oceanic distribution of prasinophytes clade VII, the dominant group of green algae in oceanic waters. ISME J. 2017;11:512–28.
Egge ES, Johannessen TV, Andersen T, Eikrem W, Bittner L, Larsen A, et al. Seasonal diversity and dynamics of haptophytes in the Skagerrak, Norway, explored by high-throughput sequencing. Mol Ecol. 2015;24:3026–42.
Ichinomiya M, dos Santos AL, Gourvil P, Yoshikawa S, Kamiya M, Ohki K, et al. Diversity and oceanic distribution of the Parmales (Bolidophyceae), a picoplanktonic group closely related to diatoms. ISME J. 2016;10:2419–34.
Zouari AB, Hassen MB, Balague V, Sahli E, Ben Kacem MY, Akrout F, et al. Picoeukaryotic diversity in the Gulf of Gabes: variability patterns and relationships to nutrients and water masses. Aquat Microb Ecol. 2018;81:37–53.
Zhu F, Massana R, Not F, Marie D, Vaulot D. Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol. 2005;52:79–92.
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). Env Microbiol. 2008;10:3349–65.
Lie AAY, Kim DY, Schnetzer A, Caron DA. Small-scale temporal and spatial variations in protistan community composition at the San Pedro Ocean Time-series station off the coast of southern California. Aquat Microb Ecol. 2013;70:93–110.
Anderson OR. Radiolaria. New York: Springer; 1983.
Suzuki N, Ogane K, Aita Y, Kato M, Sakai S, Kurihara T, et al. Distribution patterns of the radiolarian nuclei and symbionts using DAPI-fluorescence. Bull Natl Mus Nat Sci Ser B. 2009;169–82.
Suzuki N, Aita Y. Radiolaria: achievements and unresolved issues: taxonomy and cytology. Plankt Benthos Res. 2011;6:69–91.
Biard T, Bigeard E, Audic S, Poulain J, Gutierrez-Rodriguez A, Pesant S, et al. Biogeography and diversity of Collodaria (Radiolaria) in the global ocean. ISME J. 2017;11:1331–44.
Decelle J, Romac S, Sasaki E, Not F, Mahé F. Intracellular diversity of the V4 and V9 regions of the 18S rRNA in marine protists (radiolarians) assessed by high-throughput sequencing. PLoS One. 2014;9:e104297.
Godhe A, Asplund ME, Harnstrom K, Saravanan V, Tyagi A, Karunasagar I. Quantification of diatom and dinoflagellate biomasses in coastal marine seawater samples by real-time PCR. Appl Env Microbiol. 2008;74:7174–82.
Giner CR, Forn I, Romac S, Logares R, De Vargas C, Massana R. Environmental sequencing provides reasonable estimates of the relative abundance of specific picoeukaryotes. Appl Environ Microbiol. 2016;82:4757–66.
Boltovskoy D. Vertical distribution patterns of Radiolaria Polycystina (Protista) in the World Ocean: living ranges, isothermal submersion and settling shells. J Plankton Res. 2017;39:330–49.
Decelle J, Martin P, Paborstava K, Pond DW, Tarling G, Mahé F, et al. Diversity, Ecology and Biogeochemistry of Cyst-Forming Acantharia (Radiolaria) in the Oceans. PLoS One. 2013;8:e53598.
Gowing MM, Coale SL. Fluxes of living radiolarians and their skeletons along a northeast Pacific transect from coastal upwelling to open ocean waters. Deep Sea Res Part A-Oceanogr Res Pap. 1989;36:561–76.
Takahashi K. Radiolaria - sinking population, standing stock, and production-rate. Mar Micropaleontol. 1983;8:171–81.
Dennett MR, Caron DA, Michaels AF, Gallager SM, Davis CS. Video plankton recorder reveals high abundances of colonial Radiolaria in surface waters of the central North Pacific. J Plankton Res. 2002;24:797–805.
Suzuki N, Not F. Biology and Ecology of Radiolaria. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F (eds). pp. 179–222, Springer: Japan; 2015.
Takahashi K. Radiolarian flux and seasonality: climatic and El Niño response in the subarctic Pacific, 1982-4. Glob Biogeochem Cycles. 1987;1:213–31.
Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature. 2016;532:465–70.
Gowing MM. Trophic biology of phaeodarian radiolarians and flux of living radiolarians in the upper 2000-m of the North Pacific Central Gyre. Deep Sea Res Part A- Oceanogr Res Pap. 1986;33:655–74.
Ohman MD, Powell JR, Picheral M, Jensen DW. Mesozooplankton and particulate matter responses to a deep-water frontal system in the southern California Current System. J Plankton Res. 2012;34:815–27.
Biard T, Stemmann L, Picheral M, Mayot N, Vandromme P, Hauss H, et al. In situ imaging reveals the biomass of giant protists in the global ocean. Nature. 2016;532:504–7.
Bond NA, Cronin MF, Freeland H, Mantua N. Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys Res Lett. 2015;42:3414–20.
Gentemann CL, Fewings MR, García-Reyes M. Satellite sea surface temperatures along the West Coast of the United States during the 2014-6 northeast Pacific marine heat wave. Geophys Res Lett. 2017;44:312–9.
Peterson WT, Fisher JL, Strub PT, Du X, Risien C, Peterson J, et al. The pelagic ecosystem in the Northern California Current off Oregon during the 2014-6 warm anomalies within the context of the past 20 years. J Geophys Res Ocean. 2017;122:7267–90.
Gómez F, Qiu D, Dodge JD, Lopes RM, Lin S. Morphological and molecular characterization of Ptychodiscus noctiluca revealed the polyphyletic nature of the order Ptychodiscales (Dinophyceae). J Phycol. 2016;52:793–805.
Stukel MR, Biard T, Krause J, Ohman MD. Large Phaeodaria in the twilight zone: Their role in the carbon cycle. Limnol Oceanogr. 2018;63:2579–94
Biard T, Krause JW, Stukel MR, Ohman MD. The significance of giant phaeodarians (Rhizaria) to biogenic silica export in the California Current Ecosystem. Glob Biogeochem Cycles. 2018;32:987–1004.
Taylor GT, Karl DM, Pace ML. Impact of bacteria and zooflagellates on the composition of sinking particles: an in situ experiment. Mar Ecol Prog Ser. 1986;29:141–55.
Iversen MH, Poulsen LK. Coprorhexy, coprophagy, and coprochaly in the copepods Calanus helgolandicus, Pseudocalanus elongatus, and Oithona similis. Mar Ecol Prog Ser. 2007;350:79–89.
Noji TT. The influence of macrozooplankton on vertical particulate flux. Sarsia. 1991;76:1–9.
Mayor DJ, Sanders R, Giering SL, Anderson TR. Microbial gardening in theocean’s twilight zone: detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus: fragmentation of refractory detritus by zooplankton beneath the euphotic zone stimulates the harvestable productio. Bioessays. 2014;36:1132–7.
Lim EL, Dennett MR, Caron DA. The ecology of Paraphysomonas imperforate based on studies employing oligonucleotide probe identification in coastal water samples and enrichment cultures. Limnol Oceanogr. 1999;44:37–51.
Caron DA, Davis PG, Madin LP, Sieburth JM. Heterotrophic bacteria and bacterivorous protozoa in oceanic macro-aggregates. Science. 1982;218:795–7.
Silver MW, Gowing MM, Brownlee DC, Corliss JO. Ciliated protozoa associated with oceanic sinking detritus. Nature. 1984;309:246–8.
Gowing MM, Bentham WN. Feeding ecology of phaeodarian radiolarians at the VERTEX North Pacific time-series site. J Plankton Res. 1994;16:707–19.
Not F, del Campo J, Balagué V, De Vargas C, Massana R. New insights into the diversity of marine picoeukaryotes. PLoS One. 2009;4:e7143.
Stemmann L, Youngbluth M, Robert K, Hosia A, Picheral M, Paterson H, et al. Global zoogeography of fragile macrozooplankton in the upper 100–1000 m inferred from the underwater video profiler. ICES J Mar Sci. 2008;65:433–42.
Acknowledgements
We would like to acknowledge Estelle Bigeard for her help during the DNA extraction and Illumina library preparation, Ralf Goericke for the Chl a and nutrient data, and the crew and research technicians of RV Melville for their assistance during the CCE-P1408 Process Cruise. CCE-LTER ship and science support were provided by NSF grants OCE-1026607 and OCE-1637632. We are grateful to the Genomer and ABIMS platforms for access to the Illumina sequencer and bioinformatic cluster, Brittany region SAD grant SYMBIOX for funding AGR research and Sorbonne Universités Emergence grant to FN, NIWA for its support to AGR during data analysis and writing of the manuscript via New Zealand Strategic Science Investment Funding to the National Coasts & Oceans Centre, and Scott Nodder (NIWA) for support and fruitful discussions. Funds for ALS was provided by FONDECYT grant PiSCO South (N1171802).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Gutierrez-Rodriguez, A., Stukel, M.R., Lopes dos Santos, A. et al. High contribution of Rhizaria (Radiolaria) to vertical export in the California Current Ecosystem revealed by DNA metabarcoding. ISME J 13, 964–976 (2019). https://doi.org/10.1038/s41396-018-0322-7
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-018-0322-7
This article is cited by
-
Marine heatwaves modulate food webs and carbon transport processes
Nature Communications (2025)
-
Inventorizing marine biodiversity using eDNA data from Indonesian coral reefs: comparative high throughput analysis using different bioinformatic pipelines
Marine Biodiversity (2024)
-
Water masses shape pico-nano eukaryotic communities of the Weddell Sea
Communications Biology (2023)
-
Tracing the path of carbon export in the ocean though DNA sequencing of individual sinking particles
The ISME Journal (2022)
-
Contrasting sea ice conditions shape microbial food webs in Hudson Bay (Canadian Arctic)
ISME Communications (2022)
