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Research Article

Microbial dynamics of elevated carbon flux in the open ocean’s abyss

Kirsten E. Poff, Andy O. Leu, View ORCID ProfileJohn M. Eppley, View ORCID ProfileDavid M. Karl, and View ORCID ProfileEdward F. DeLong
  1. aDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaiʻi at Mānoa, Honolulu, HI 96822

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PNAS January 26, 2021 118 (4) e2018269118; https://doi.org/10.1073/pnas.2018269118
Kirsten E. Poff
aDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaiʻi at Mānoa, Honolulu, HI 96822
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Andy O. Leu
aDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaiʻi at Mānoa, Honolulu, HI 96822
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John M. Eppley
aDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaiʻi at Mānoa, Honolulu, HI 96822
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  • ORCID record for John M. Eppley
David M. Karl
aDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaiʻi at Mānoa, Honolulu, HI 96822
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Edward F. DeLong
aDaniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaiʻi at Mānoa, Honolulu, HI 96822
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  • For correspondence: edelong@hawaii.edu
  1. Contributed by Edward F. DeLong, December 17, 2020 (sent for review August 31, 2020; reviewed by Otto X. Cordero and Byron C. Crump)

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Significance

The ocean’s “biological pump” exports sinking particles containing carbon, nutrients, and energy to the deep sea, contributing centrally to the global carbon cycle. Here, we identify key organisms and biological processes associated with elevated carbon flux to the abyss. Our analyses reveal that, during summer export, specific populations of photosynthetic algae, heterotrophic protists, and bacteria reach the abyss on sinking particles. Deep-sea bacteria respond rapidly to this elevated nutrient delivery to the abyss in summer. During other seasons, different organisms and processes appear responsible for particle export to the deep sea. Our analyses reveal key biota and biological processes that interconnect surface productivity, particle export, and the deep-sea ecosystem, thereby influencing the function and efficiency of the ocean’s biological pump.

Abstract

In the open ocean, elevated carbon flux (ECF) events increase the delivery of particulate carbon from surface waters to the seafloor by severalfold compared to other times of year. Since microbes play central roles in primary production and sinking particle formation, they contribute greatly to carbon export to the deep sea. Few studies, however, have quantitatively linked ECF events with the specific microbial assemblages that drive them. Here, we identify key microbial taxa and functional traits on deep-sea sinking particles that correlate positively with ECF events. Microbes enriched on sinking particles in summer ECF events included symbiotic and free-living diazotrophic cyanobacteria, rhizosolenid diatoms, phototrophic and heterotrophic protists, and photoheterotrophic and copiotrophic bacteria. Particle-attached bacteria reaching the abyss during summer ECF events encoded metabolic pathways reflecting their surface water origins, including oxygenic and aerobic anoxygenic photosynthesis, nitrogen fixation, and proteorhodopsin-based photoheterotrophy. The abundances of some deep-sea bacteria also correlated positively with summer ECF events, suggesting rapid bathypelagic responses to elevated organic matter inputs. Biota enriched on sinking particles during a spring ECF event were distinct from those found in summer, and included rhizaria, copepods, fungi, and different bacterial taxa. At other times over our 3-y study, mid- and deep-water particle colonization, predation, degradation, and repackaging (by deep-sea bacteria, protists, and animals) appeared to shape the biotic composition of particles reaching the abyss. Our analyses reveal key microbial players and biological processes involved in particle formation, rapid export, and consumption, that may influence the ocean’s biological pump and help sustain deep-sea ecosystems.

  • carbon export
  • biological carbon pump
  • deep sea
  • marine microbes
  • open ocean

Footnotes

  • ↵1K.E.P. and A.O.L. contributed equally to the work.

  • ↵2To whom correspondence may be addressed. Email: edelong{at}hawaii.edu.
  • Author contributions: D.M.K. and E.F.D. designed research; K.E.P., A.O.L., J.M.E., and E.F.D. performed research; K.E.P., A.O.L., J.M.E., D.M.K., and E.F.D. analyzed data; and K.E.P., A.O.L., J.M.E., D.M.K., and E.F.D. wrote the paper.

  • Reviewers: O.X.C., Massachusetts Institute of Technology; and B.C.C., Oregon State University.

  • The authors declare no competing interest.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2018269118/-/DCSupplemental.

Data Availability.

Sequence read data are available from the National Center for Biotechnology Information (NCBI) short read archive (SRA) under Bioproject no. PRJNA482655. Individual MAGs are available under NCBI accession nos. SAMN14675689 to SAMN14675809. All other data products associated with this study are available from the corresponding author upon request.

  • Copyright © 2021 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Microbial dynamics of elevated carbon flux in the open ocean’s abyss
Kirsten E. Poff, Andy O. Leu, John M. Eppley, David M. Karl, Edward F. DeLong
Proceedings of the National Academy of Sciences Jan 2021, 118 (4) e2018269118; DOI: 10.1073/pnas.2018269118

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Microbial dynamics of elevated carbon flux in the open ocean’s abyss
Kirsten E. Poff, Andy O. Leu, John M. Eppley, David M. Karl, Edward F. DeLong
Proceedings of the National Academy of Sciences Jan 2021, 118 (4) e2018269118; DOI: 10.1073/pnas.2018269118
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Proceedings of the National Academy of Sciences: 118 (4)
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