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Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments

Gomaa, Fatma ; Utter, Daniel R. ; Powers, Christopher ; Beaudoin, David J. ; Edgcomb, Virginia P. ; Filipsson, Helena L. LU orcid ; Hansel, Colleen M. ; Wankel, Scott D. ; Zhang, Ying and Bernhard, Joan M. (2021) In Science Advances 7(22).
Abstract

Oceanic deoxygenation is increasingly affecting marine ecosystems; many taxa will be severely challenged, yet certain nominally aerobic foraminifera (rhizarian protists) thrive in oxygen-depleted to anoxic, sometimes sulfidic, sediments uninhabitable to most eukaryotes. Gene expression analyses of foraminifera common to severely hypoxic or anoxic sediments identified metabolic strategies used by this abundant taxon. In field-collected and laboratory-incubated samples, foraminifera expressed denitrification genes regardless of oxygen regime with a putative nitric oxide dismutase, a characteristic enzyme of oxygenic denitrification. A pyruvate:ferredoxin oxidoreductase was highly expressed, indicating the capability for anaerobic energy... (More)

Oceanic deoxygenation is increasingly affecting marine ecosystems; many taxa will be severely challenged, yet certain nominally aerobic foraminifera (rhizarian protists) thrive in oxygen-depleted to anoxic, sometimes sulfidic, sediments uninhabitable to most eukaryotes. Gene expression analyses of foraminifera common to severely hypoxic or anoxic sediments identified metabolic strategies used by this abundant taxon. In field-collected and laboratory-incubated samples, foraminifera expressed denitrification genes regardless of oxygen regime with a putative nitric oxide dismutase, a characteristic enzyme of oxygenic denitrification. A pyruvate:ferredoxin oxidoreductase was highly expressed, indicating the capability for anaerobic energy generation during exposure to hypoxia and anoxia. Near-complete expression of a diatom’s plastid genome in one foraminiferal species suggests kleptoplasty or sequestration of functional plastids, conferring a metabolic advantage despite the host living far below the euphotic zone. Through a unique integration of functions largely unrecognized among “typical” eukaryotes, benthic foraminifera represent winning microeukaryotes in the face of ongoing oceanic deoxygenation.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Science Advances
volume
7
issue
22
article number
eabf1586
publisher
American Association for the Advancement of Science (AAAS)
external identifiers
  • scopus:85106553386
  • pmid:34039603
ISSN
2375-2548
DOI
10.1126/sciadv.abf1586
language
English
LU publication?
yes
id
c7cf653f-1ab1-4891-b3a1-14a082746db4
date added to LUP
2021-06-09 11:21:04
date last changed
2024-06-15 12:14:46
@article{c7cf653f-1ab1-4891-b3a1-14a082746db4,
  abstract     = {{<p>Oceanic deoxygenation is increasingly affecting marine ecosystems; many taxa will be severely challenged, yet certain nominally aerobic foraminifera (rhizarian protists) thrive in oxygen-depleted to anoxic, sometimes sulfidic, sediments uninhabitable to most eukaryotes. Gene expression analyses of foraminifera common to severely hypoxic or anoxic sediments identified metabolic strategies used by this abundant taxon. In field-collected and laboratory-incubated samples, foraminifera expressed denitrification genes regardless of oxygen regime with a putative nitric oxide dismutase, a characteristic enzyme of oxygenic denitrification. A pyruvate:ferredoxin oxidoreductase was highly expressed, indicating the capability for anaerobic energy generation during exposure to hypoxia and anoxia. Near-complete expression of a diatom’s plastid genome in one foraminiferal species suggests kleptoplasty or sequestration of functional plastids, conferring a metabolic advantage despite the host living far below the euphotic zone. Through a unique integration of functions largely unrecognized among “typical” eukaryotes, benthic foraminifera represent winning microeukaryotes in the face of ongoing oceanic deoxygenation.</p>}},
  author       = {{Gomaa, Fatma and Utter, Daniel R. and Powers, Christopher and Beaudoin, David J. and Edgcomb, Virginia P. and Filipsson, Helena L. and Hansel, Colleen M. and Wankel, Scott D. and Zhang, Ying and Bernhard, Joan M.}},
  issn         = {{2375-2548}},
  language     = {{eng}},
  number       = {{22}},
  publisher    = {{American Association for the Advancement of Science (AAAS)}},
  series       = {{Science Advances}},
  title        = {{Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments}},
  url          = {{http://dx.doi.org/10.1126/sciadv.abf1586}},
  doi          = {{10.1126/sciadv.abf1586}},
  volume       = {{7}},
  year         = {{2021}},
}