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

ABSTRACT 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 su...

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Autores principales: Vega Shah, Xiaowei Zhao, Rachel A. Lundeen, Anitra E. Ingalls, Daniela Nicastro, Robert M. Morris
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Lenguaje:EN
Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:6e0f1facba894b419ff7e1de5e2c92b82021-11-15T15:55:24ZMorphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation10.1128/mBio.00216-192150-7511https://doaj.org/article/6e0f1facba894b419ff7e1de5e2c92b82019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00216-19https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE 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.Vega ShahXiaowei ZhaoRachel A. LundeenAnitra E. IngallsDaniela NicastroRobert M. MorrisAmerican Society for MicrobiologyarticleOMZSUP05chemoautotrophyoxygensulfurMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution DOAJ
collection DOAJ
language EN
topic OMZ
SUP05
chemoautotrophy
oxygen
sulfur
Microbiology
QR1-502
spellingShingle OMZ
SUP05
chemoautotrophy
oxygen
sulfur
Microbiology
QR1-502
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
description ABSTRACT 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. IMPORTANCE 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.
format article
author Vega Shah
Xiaowei Zhao
Rachel A. Lundeen
Anitra E. Ingalls
Daniela Nicastro
Robert M. Morris
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
publishDate 2019
url https://doaj.org/article/6e0f1facba894b419ff7e1de5e2c92b8
work_keys_str_mv AT vegashah morphologicalplasticityinasulfuroxidizingmarinebacteriumfromthesup05cladeenhancesdarkcarbonfixation
AT xiaoweizhao morphologicalplasticityinasulfuroxidizingmarinebacteriumfromthesup05cladeenhancesdarkcarbonfixation
AT rachelalundeen morphologicalplasticityinasulfuroxidizingmarinebacteriumfromthesup05cladeenhancesdarkcarbonfixation
AT anitraeingalls morphologicalplasticityinasulfuroxidizingmarinebacteriumfromthesup05cladeenhancesdarkcarbonfixation
AT danielanicastro morphologicalplasticityinasulfuroxidizingmarinebacteriumfromthesup05cladeenhancesdarkcarbonfixation
AT robertmmorris morphologicalplasticityinasulfuroxidizingmarinebacteriumfromthesup05cladeenhancesdarkcarbonfixation
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