Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation

Identifying shifts in microbial metabolism across redox gradients will improve efforts to model marine oxygen minimum zone (OMZ) ecosystems. Here, we show that aerobic morphology and metabolism increase cell size, sulfur storage capacity, and carbon fixation rates in “Ca. Thioglobus autotrophicus,”...

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Main Authors: Vega Shah, Xiaowei Zhao, Rachel A. Lundeen, Anitra E. Ingalls, Daniela Nicastro, Robert M. Morris
Format: Article
Language:English
Published: American Society for Microbiology 2019-05-01
Series:mBio
Subjects:
OMZ
Online Access:https://doi.org/10.1128/mBio.00216-19
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spelling doaj-f22d693692f54a32842078831b56a04e2021-07-02T04:40:44ZengAmerican Society for MicrobiologymBio2150-75112019-05-01103e00216-1910.1128/mBio.00216-19Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon FixationVega ShahXiaowei ZhaoRachel A. LundeenAnitra E. IngallsDaniela NicastroRobert M. MorrisIdentifying shifts in microbial metabolism across redox gradients will improve efforts to model marine oxygen minimum zone (OMZ) ecosystems. Here, we show that aerobic morphology and metabolism increase cell size, sulfur storage capacity, and carbon fixation rates in “Ca. Thioglobus autotrophicus,” a chemosynthetic bacterium from the SUP05 clade that crosses oxic-anoxic boundaries.Sulfur-oxidizing bacteria from the SUP05 clade are abundant in anoxic and oxygenated marine waters that appear to lack reduced sources of sulfur for cell growth. This raises questions about how these chemosynthetic bacteria survive across oxygen and sulfur gradients and how their mode of survival impacts the environment. Here, we use growth experiments, proteomics, and cryo-electron tomography to show that a SUP05 isolate, “Candidatus Thioglobus autotrophicus,” is amorphous in shape and several times larger and stores considerably more intracellular sulfur when it respires oxygen. We also show that these cells can use diverse sources of reduced organic and inorganic sulfur at submicromolar concentrations. Enhanced cell size, carbon content, and metabolic activity of the aerobic phenotype are likely facilitated by a stabilizing surface-layer (S-layer) and an uncharacterized form of FtsZ-less cell division that supports morphological plasticity. The additional sulfur storage provides an energy source that allows cells to continue metabolic activity when exogenous sulfur sources are not available. This metabolic flexibility leads to the production of more organic carbon in the ocean than is estimated based solely on their anaerobic phenotype.https://doi.org/10.1128/mBio.00216-19OMZSUP05chemoautotrophyoxygensulfur
collection DOAJ
language English
format Article
sources DOAJ
author Vega Shah
Xiaowei Zhao
Rachel A. Lundeen
Anitra E. Ingalls
Daniela Nicastro
Robert M. Morris
spellingShingle Vega Shah
Xiaowei Zhao
Rachel A. Lundeen
Anitra E. Ingalls
Daniela Nicastro
Robert M. Morris
Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation
mBio
OMZ
SUP05
chemoautotrophy
oxygen
sulfur
author_facet Vega Shah
Xiaowei Zhao
Rachel A. Lundeen
Anitra E. Ingalls
Daniela Nicastro
Robert M. Morris
author_sort Vega Shah
title Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation
title_short Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation
title_full Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation
title_fullStr Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation
title_full_unstemmed Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation
title_sort morphological plasticity in a sulfur-oxidizing marine bacterium from the sup05 clade enhances dark carbon fixation
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2019-05-01
description Identifying shifts in microbial metabolism across redox gradients will improve efforts to model marine oxygen minimum zone (OMZ) ecosystems. Here, we show that aerobic morphology and metabolism increase cell size, sulfur storage capacity, and carbon fixation rates in “Ca. Thioglobus autotrophicus,” a chemosynthetic bacterium from the SUP05 clade that crosses oxic-anoxic boundaries.Sulfur-oxidizing bacteria from the SUP05 clade are abundant in anoxic and oxygenated marine waters that appear to lack reduced sources of sulfur for cell growth. This raises questions about how these chemosynthetic bacteria survive across oxygen and sulfur gradients and how their mode of survival impacts the environment. Here, we use growth experiments, proteomics, and cryo-electron tomography to show that a SUP05 isolate, “Candidatus Thioglobus autotrophicus,” is amorphous in shape and several times larger and stores considerably more intracellular sulfur when it respires oxygen. We also show that these cells can use diverse sources of reduced organic and inorganic sulfur at submicromolar concentrations. Enhanced cell size, carbon content, and metabolic activity of the aerobic phenotype are likely facilitated by a stabilizing surface-layer (S-layer) and an uncharacterized form of FtsZ-less cell division that supports morphological plasticity. The additional sulfur storage provides an energy source that allows cells to continue metabolic activity when exogenous sulfur sources are not available. This metabolic flexibility leads to the production of more organic carbon in the ocean than is estimated based solely on their anaerobic phenotype.
topic OMZ
SUP05
chemoautotrophy
oxygen
sulfur
url https://doi.org/10.1128/mBio.00216-19
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