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Title: RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon

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. Themore » RcaE photoreceptor links perception of external light cues to regulating carboxysome structure and function and, thus, to the cellular capacity for carbon fixation.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [3];
  1. Department of Energy—Plant Research Laboratory, Michigan State University, Plant Biology Laboratories, East Lansing, Michigan, USA, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan, USA
  2. Department of Energy—Plant Research Laboratory, Michigan State University, Plant Biology Laboratories, East Lansing, Michigan, USA
  3. Department of Energy—Plant Research Laboratory, Michigan State University, Plant Biology Laboratories, East Lansing, Michigan, USA, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan, USA, Department of Microbiology & Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
OSTI Identifier:
1493949
Alternate Identifier(s):
OSTI ID: 1511019
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Published Article
Journal Name:
mSphere
Additional Journal Information:
Journal Name: mSphere Journal Volume: 3 Journal Issue: 1; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carbon-concentrating mechanism (CCM); carboxysome; cyanobacteria; light signaling; photomorphogenesis; photosynthesis

Citation Formats

Rohnke, Brandon A., Singh, Shailendra P., Pattanaik, Bagmi, Montgomery, Beronda L., and Ellermeier, ed., Craig D. RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon. United States: N. p., 2018. Web. doi:10.1128/mSphere.00617-17.
Rohnke, Brandon A., Singh, Shailendra P., Pattanaik, Bagmi, Montgomery, Beronda L., & Ellermeier, ed., Craig D. RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon. United States. https://doi.org/10.1128/mSphere.00617-17
Rohnke, Brandon A., Singh, Shailendra P., Pattanaik, Bagmi, Montgomery, Beronda L., and Ellermeier, ed., Craig D. Wed . "RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon". United States. https://doi.org/10.1128/mSphere.00617-17.
@article{osti_1493949,
title = {RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon},
author = {Rohnke, Brandon A. and Singh, Shailendra P. and Pattanaik, Bagmi and Montgomery, Beronda L. and Ellermeier, ed., Craig D.},
abstractNote = {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.},
doi = {10.1128/mSphere.00617-17},
journal = {mSphere},
number = 1,
volume = 3,
place = {United States},
year = {Wed Jan 24 00:00:00 EST 2018},
month = {Wed Jan 24 00:00:00 EST 2018}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1128/mSphere.00617-17

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