RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>

ABSTRACT Carboxysomes are central to the carbon dioxide-concentrating mechanism (CCM) and carbon fixation in cyanobacteria. Although the structure is well understood, roles of environmental cues in the synthesis, positioning, and functional tuning of carboxysomes have not been systematically studied...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Brandon A. Rohnke, Shailendra P. Singh, Bagmi Pattanaik, Beronda L. Montgomery
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	carbon-concentrating mechanism (CCM) carboxysome cyanobacteria light signaling photomorphogenesis photosynthesis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2a04e879f69e4c5abd4a904cc8a5c77c
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:2a04e879f69e4c5abd4a904cc8a5c77c
record_format	dspace
spelling	oai:doaj.org-article:2a04e879f69e4c5abd4a904cc8a5c77c2021-11-15T15:22:02ZRcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>10.1128/mSphere.00617-172379-5042https://doaj.org/article/2a04e879f69e4c5abd4a904cc8a5c77c2018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00617-17https://doaj.org/toc/2379-5042ABSTRACT Carboxysomes are central to the carbon dioxide-concentrating mechanism (CCM) and carbon fixation in cyanobacteria. Although the structure is well understood, roles of environmental cues in the synthesis, positioning, and functional tuning of carboxysomes have not been systematically studied. Fremyella diplosiphon is a model cyanobacterium for assessing impacts of environmental light cues on photosynthetic pigmentation and tuning of photosynthetic efficiency during complementary chromatic acclimation (CCA), which is controlled by the photoreceptor RcaE. Given the central role of carboxysomes in photosynthesis, we investigated roles of light-dependent RcaE signaling in carboxysome structure and function. A ΔrcaE mutant exhibits altered carboxysome size and number, ccm gene expression, and carboxysome protein accumulation relative to the wild-type (WT) strain. Several Ccm proteins, including carboxysome shell proteins and core-nucleating factors, overaccumulate in ΔrcaE cells relative to WT cells. Additionally, levels of carboxysome cargo RuBisCO in the ΔrcaE mutant are lower than or unchanged from those in the WT strain. This shift in the ratios of carboxysome shell and nucleating components to the carboxysome cargo appears to drive carboxysome morphology and abundance dynamics. Carboxysomes are also occasionally mislocalized spatially to the periphery of spherical mutants within thylakoid membranes, suggesting that carboxysome positioning is impacted by cell shape. The RcaE photoreceptor links perception of external light cues to regulating carboxysome structure and function and, thus, to the cellular capacity for carbon fixation. IMPORTANCE Carboxysomes are proteinaceous subcellular compartments, or bacterial organelles, found in cyanobacteria that consist of a protein shell surrounding a core primarily composed of the enzyme ribulose-1,5-biphosphate carboxylase/oxygenase (RuBisCO) that is central to the carbon dioxide-concentrating mechanism (CCM) and carbon fixation. Whereas significant insights have been gained regarding the structure and synthesis of carboxysomes, limited attention has been given to how their size, abundance, and protein composition are regulated to ensure optimal carbon fixation in dynamic environments. Given the centrality of carboxysomes in photosynthesis, we provide an analysis of the role of a photoreceptor, RcaE, which functions in matching photosynthetic pigmentation to the external environment during complementary chromatic acclimation and thereby optimizing photosynthetic efficiency, in regulating carboxysome dynamics. Our data highlight a role for RcaE in perceiving external light cues and regulating carboxysome structure and function and, thus, in the cellular capacity for carbon fixation and organismal fitness.Brandon A. RohnkeShailendra P. SinghBagmi PattanaikBeronda L. MontgomeryAmerican Society for Microbiologyarticlecarbon-concentrating mechanism (CCM)carboxysomecyanobacterialight signalingphotomorphogenesisphotosynthesisMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbon-concentrating mechanism (CCM) carboxysome cyanobacteria light signaling photomorphogenesis photosynthesis Microbiology QR1-502
spellingShingle	carbon-concentrating mechanism (CCM) carboxysome cyanobacteria light signaling photomorphogenesis photosynthesis Microbiology QR1-502 Brandon A. Rohnke Shailendra P. Singh Bagmi Pattanaik Beronda L. Montgomery RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>
description	ABSTRACT Carboxysomes are central to the carbon dioxide-concentrating mechanism (CCM) and carbon fixation in cyanobacteria. Although the structure is well understood, roles of environmental cues in the synthesis, positioning, and functional tuning of carboxysomes have not been systematically studied. Fremyella diplosiphon is a model cyanobacterium for assessing impacts of environmental light cues on photosynthetic pigmentation and tuning of photosynthetic efficiency during complementary chromatic acclimation (CCA), which is controlled by the photoreceptor RcaE. Given the central role of carboxysomes in photosynthesis, we investigated roles of light-dependent RcaE signaling in carboxysome structure and function. A ΔrcaE mutant exhibits altered carboxysome size and number, ccm gene expression, and carboxysome protein accumulation relative to the wild-type (WT) strain. Several Ccm proteins, including carboxysome shell proteins and core-nucleating factors, overaccumulate in ΔrcaE cells relative to WT cells. Additionally, levels of carboxysome cargo RuBisCO in the ΔrcaE mutant are lower than or unchanged from those in the WT strain. This shift in the ratios of carboxysome shell and nucleating components to the carboxysome cargo appears to drive carboxysome morphology and abundance dynamics. Carboxysomes are also occasionally mislocalized spatially to the periphery of spherical mutants within thylakoid membranes, suggesting that carboxysome positioning is impacted by cell shape. The RcaE photoreceptor links perception of external light cues to regulating carboxysome structure and function and, thus, to the cellular capacity for carbon fixation. IMPORTANCE Carboxysomes are proteinaceous subcellular compartments, or bacterial organelles, found in cyanobacteria that consist of a protein shell surrounding a core primarily composed of the enzyme ribulose-1,5-biphosphate carboxylase/oxygenase (RuBisCO) that is central to the carbon dioxide-concentrating mechanism (CCM) and carbon fixation. Whereas significant insights have been gained regarding the structure and synthesis of carboxysomes, limited attention has been given to how their size, abundance, and protein composition are regulated to ensure optimal carbon fixation in dynamic environments. Given the centrality of carboxysomes in photosynthesis, we provide an analysis of the role of a photoreceptor, RcaE, which functions in matching photosynthetic pigmentation to the external environment during complementary chromatic acclimation and thereby optimizing photosynthetic efficiency, in regulating carboxysome dynamics. Our data highlight a role for RcaE in perceiving external light cues and regulating carboxysome structure and function and, thus, in the cellular capacity for carbon fixation and organismal fitness.
format	article
author	Brandon A. Rohnke Shailendra P. Singh Bagmi Pattanaik Beronda L. Montgomery
author_facet	Brandon A. Rohnke Shailendra P. Singh Bagmi Pattanaik Beronda L. Montgomery
author_sort	Brandon A. Rohnke
title	RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>
title_short	RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>
title_full	RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>
title_fullStr	RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>
title_full_unstemmed	RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>
title_sort	rcae-dependent regulation of carboxysome structural proteins has a central role in environmental determination of carboxysome morphology and abundance in <italic toggle="yes">fremyella diplosiphon</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/2a04e879f69e4c5abd4a904cc8a5c77c
work_keys_str_mv	AT brandonarohnke rcaedependentregulationofcarboxysomestructuralproteinshasacentralroleinenvironmentaldeterminationofcarboxysomemorphologyandabundanceinitalictoggleyesfremyelladiplosiphonitalic AT shailendrapsingh rcaedependentregulationofcarboxysomestructuralproteinshasacentralroleinenvironmentaldeterminationofcarboxysomemorphologyandabundanceinitalictoggleyesfremyelladiplosiphonitalic AT bagmipattanaik rcaedependentregulationofcarboxysomestructuralproteinshasacentralroleinenvironmentaldeterminationofcarboxysomemorphologyandabundanceinitalictoggleyesfremyelladiplosiphonitalic AT berondalmontgomery rcaedependentregulationofcarboxysomestructuralproteinshasacentralroleinenvironmentaldeterminationofcarboxysomemorphologyandabundanceinitalictoggleyesfremyelladiplosiphonitalic
_version_	1718428060115533824

RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in <italic toggle="yes">Fremyella diplosiphon</italic>

Ejemplares similares