SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter

ABSTRACT Deep-ocean regions beyond the reach of sunlight contain an estimated 615 Pg of dissolved organic matter (DOM), much of which persists for thousands of years. It is thought that bacteria oxidize DOM until it is too dilute or refractory to support microbial activity. We analyzed five single-a...

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Autores principales: Zachary Landry, Brandon K. Swan, Gerhard J. Herndl, Ramunas Stepanauskas, Stephen J. Giovannoni
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:10f8eacdbc3347819b8bcf7734eddd292021-11-15T15:51:00ZSAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter10.1128/mBio.00413-172150-7511https://doaj.org/article/10f8eacdbc3347819b8bcf7734eddd292017-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00413-17https://doaj.org/toc/2150-7511ABSTRACT Deep-ocean regions beyond the reach of sunlight contain an estimated 615 Pg of dissolved organic matter (DOM), much of which persists for thousands of years. It is thought that bacteria oxidize DOM until it is too dilute or refractory to support microbial activity. We analyzed five single-amplified genomes (SAGs) from the abundant SAR202 clade of dark-ocean bacterioplankton and found they encode multiple families of paralogous enzymes involved in carbon catabolism, including several families of oxidative enzymes that we hypothesize participate in the degradation of cyclic alkanes. The five partial genomes encoded 152 flavin mononucleotide/F420-dependent monooxygenases (FMNOs), many of which are predicted to be type II Baeyer-Villiger monooxygenases (BVMOs) that catalyze oxygen insertion into semilabile alicyclic alkanes. The large number of oxidative enzymes, as well as other families of enzymes that appear to play complementary roles in catabolic pathways, suggests that SAR202 might catalyze final steps in the biological oxidation of relatively recalcitrant organic compounds to refractory compounds that persist. IMPORTANCE Carbon in the ocean is massively sequestered in a complex mixture of biologically refractory molecules that accumulate as the chemical end member of biological oxidation and diagenetic change. However, few details are known about the biochemical machinery of carbon sequestration in the deep ocean. Reconstruction of the metabolism of a deep-ocean microbial clade, SAR202, led to postulation of new biochemical pathways that may be the penultimate stages of DOM oxidation to refractory forms that persist. These pathways are tied to a proliferation of oxidative enzymes. This research illuminates dark-ocean biochemistry that is broadly consequential for reconstructing the global carbon cycle.Zachary LandryBrandon K. SwanGerhard J. HerndlRamunas StepanauskasStephen J. GiovannoniAmerican Society for MicrobiologyarticlebathypelagicChloroflexidissolved organic mattermesopelagicmonooxygenaseSAR202MicrobiologyQR1-502ENmBio, Vol 8, Iss 2 (2017)
institution DOAJ
collection DOAJ
language EN
topic bathypelagic
Chloroflexi
dissolved organic matter
mesopelagic
monooxygenase
SAR202
Microbiology
QR1-502
spellingShingle bathypelagic
Chloroflexi
dissolved organic matter
mesopelagic
monooxygenase
SAR202
Microbiology
QR1-502
Zachary Landry
Brandon K. Swan
Gerhard J. Herndl
Ramunas Stepanauskas
Stephen J. Giovannoni
SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter
description ABSTRACT Deep-ocean regions beyond the reach of sunlight contain an estimated 615 Pg of dissolved organic matter (DOM), much of which persists for thousands of years. It is thought that bacteria oxidize DOM until it is too dilute or refractory to support microbial activity. We analyzed five single-amplified genomes (SAGs) from the abundant SAR202 clade of dark-ocean bacterioplankton and found they encode multiple families of paralogous enzymes involved in carbon catabolism, including several families of oxidative enzymes that we hypothesize participate in the degradation of cyclic alkanes. The five partial genomes encoded 152 flavin mononucleotide/F420-dependent monooxygenases (FMNOs), many of which are predicted to be type II Baeyer-Villiger monooxygenases (BVMOs) that catalyze oxygen insertion into semilabile alicyclic alkanes. The large number of oxidative enzymes, as well as other families of enzymes that appear to play complementary roles in catabolic pathways, suggests that SAR202 might catalyze final steps in the biological oxidation of relatively recalcitrant organic compounds to refractory compounds that persist. IMPORTANCE Carbon in the ocean is massively sequestered in a complex mixture of biologically refractory molecules that accumulate as the chemical end member of biological oxidation and diagenetic change. However, few details are known about the biochemical machinery of carbon sequestration in the deep ocean. Reconstruction of the metabolism of a deep-ocean microbial clade, SAR202, led to postulation of new biochemical pathways that may be the penultimate stages of DOM oxidation to refractory forms that persist. These pathways are tied to a proliferation of oxidative enzymes. This research illuminates dark-ocean biochemistry that is broadly consequential for reconstructing the global carbon cycle.
format article
author Zachary Landry
Brandon K. Swan
Gerhard J. Herndl
Ramunas Stepanauskas
Stephen J. Giovannoni
author_facet Zachary Landry
Brandon K. Swan
Gerhard J. Herndl
Ramunas Stepanauskas
Stephen J. Giovannoni
author_sort Zachary Landry
title SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter
title_short SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter
title_full SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter
title_fullStr SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter
title_full_unstemmed SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter
title_sort sar202 genomes from the dark ocean predict pathways for the oxidation of recalcitrant dissolved organic matter
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/10f8eacdbc3347819b8bcf7734eddd29
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AT brandonkswan sar202genomesfromthedarkoceanpredictpathwaysfortheoxidationofrecalcitrantdissolvedorganicmatter
AT gerhardjherndl sar202genomesfromthedarkoceanpredictpathwaysfortheoxidationofrecalcitrantdissolvedorganicmatter
AT ramunasstepanauskas sar202genomesfromthedarkoceanpredictpathwaysfortheoxidationofrecalcitrantdissolvedorganicmatter
AT stephenjgiovannoni sar202genomesfromthedarkoceanpredictpathwaysfortheoxidationofrecalcitrantdissolvedorganicmatter
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