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Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms

Powers, Christopher ; Gomaa, Fatma ; Billings, Elizabeth B. ; Utter, Daniel R. ; Beaudoin, David J. ; Edgcomb, Virginia P. ; Hansel, Colleen M. ; Wankel, Scott D. ; Filipsson, Helena L. LU orcid and Zhang, Ying , et al. (2022) In Frontiers in Marine Science 9.
Abstract

Certain benthic foraminifera thrive in marine sediments with low or undetectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain elusive. To better understand the metabolic versatility of foraminifera, we studied two benthic species that thrive in oxygen-depleted marine sediments. Here we detail, via transcriptomics and metatranscriptomics, differential gene expression of Nonionella stella and Bolivina argentea, collected from Santa Barbara Basin, California, USA, in response to varied oxygenation and chemical amendments. Organelle-specific metabolic reconstructions revealed these two species utilize... (More)

Certain benthic foraminifera thrive in marine sediments with low or undetectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain elusive. To better understand the metabolic versatility of foraminifera, we studied two benthic species that thrive in oxygen-depleted marine sediments. Here we detail, via transcriptomics and metatranscriptomics, differential gene expression of Nonionella stella and Bolivina argentea, collected from Santa Barbara Basin, California, USA, in response to varied oxygenation and chemical amendments. Organelle-specific metabolic reconstructions revealed these two species utilize adaptable mitochondrial and peroxisomal metabolism. N. stella, most abundant in anoxia and characterized by lack of food vacuoles and abundance of intracellular lipid droplets, was predicted to couple the putative peroxisomal beta-oxidation and glyoxylate cycle with a versatile electron transport system and a partial TCA cycle. In contrast, B. argentea, most abundant in hypoxia and contains food vacuoles, was predicted to utilize the putative peroxisomal gluconeogenesis and a full TCA cycle but lacks the expression of key beta-oxidation and glyoxylate cycle genes. These metabolic adaptations likely confer ecological success while encountering deoxygenation and expand our understanding of metabolic modifications and interactions between mitochondria and peroxisomes in protists.

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publication status
published
subject
keywords
anoxia, benthic foraminifera, chemocline, mitochondria, peroxisomes, protists, Santa Barbara Basin
in
Frontiers in Marine Science
volume
9
article number
1010319
publisher
Frontiers Media S. A.
external identifiers
  • scopus:85144106799
ISSN
2296-7745
DOI
10.3389/fmars.2022.1010319
language
English
LU publication?
yes
id
84c23927-fbd9-44da-af57-6e79fe548431
date added to LUP
2023-01-02 10:44:34
date last changed
2023-05-10 11:23:57
@article{84c23927-fbd9-44da-af57-6e79fe548431,
  abstract     = {{<p>Certain benthic foraminifera thrive in marine sediments with low or undetectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain elusive. To better understand the metabolic versatility of foraminifera, we studied two benthic species that thrive in oxygen-depleted marine sediments. Here we detail, via transcriptomics and metatranscriptomics, differential gene expression of Nonionella stella and Bolivina argentea, collected from Santa Barbara Basin, California, USA, in response to varied oxygenation and chemical amendments. Organelle-specific metabolic reconstructions revealed these two species utilize adaptable mitochondrial and peroxisomal metabolism. N. stella, most abundant in anoxia and characterized by lack of food vacuoles and abundance of intracellular lipid droplets, was predicted to couple the putative peroxisomal beta-oxidation and glyoxylate cycle with a versatile electron transport system and a partial TCA cycle. In contrast, B. argentea, most abundant in hypoxia and contains food vacuoles, was predicted to utilize the putative peroxisomal gluconeogenesis and a full TCA cycle but lacks the expression of key beta-oxidation and glyoxylate cycle genes. These metabolic adaptations likely confer ecological success while encountering deoxygenation and expand our understanding of metabolic modifications and interactions between mitochondria and peroxisomes in protists.</p>}},
  author       = {{Powers, Christopher and Gomaa, Fatma and Billings, Elizabeth B. and Utter, Daniel R. and Beaudoin, David J. and Edgcomb, Virginia P. and Hansel, Colleen M. and Wankel, Scott D. and Filipsson, Helena L. and Zhang, Ying and Bernhard, Joan M.}},
  issn         = {{2296-7745}},
  keywords     = {{anoxia; benthic foraminifera; chemocline; mitochondria; peroxisomes; protists; Santa Barbara Basin}},
  language     = {{eng}},
  month        = {{12}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Marine Science}},
  title        = {{Two canonically aerobic foraminifera express distinct peroxisomal and mitochondrial metabolisms}},
  url          = {{http://dx.doi.org/10.3389/fmars.2022.1010319}},
  doi          = {{10.3389/fmars.2022.1010319}},
  volume       = {{9}},
  year         = {{2022}},
}