Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon
Abstract
Filamentous cyanobacterium Fremyella diplosiphon is known to alter its pigmentation and morphology during complementary chromatic acclimation (CCA) to efficiently harvest available radiant energy for photosynthesis. F. diplosiphon cells are rectangular and filaments are longer under green light (GL), whereas smaller, spherical cells and short filaments are prevalent under red light (RL). Light regulation of bolA morphogene expression is correlated with photoregulation of cellular morphology in F. diplosiphon. Here, we investigate a role for quantitative regulation of cellular BolA protein levels in morphology determination. Overexpression of bolA in WT was associated with induction of RL-characteristic spherical morphology even when cultures were grown under GL. Overexpression of bolA in a ΔrcaE background, which lacks cyanobacteriochrome photosensor RcaE and accumulates lower levels of BolA than WT, partially reverted the cellular morphology of the strain to a WT-like state. Overexpression of BolA in WT and ΔrcaE backgrounds was associated with decreased cellular reactive oxygen species (ROS) levels and an increase in filament length under both GL and RL. Morphological defects and high ROS levels commonly observed in ΔrcaE could, thus, be in part due to low accumulation of BolA. Together, these findings support an emerging model for RcaE-dependent photoregulation of BolA in controlling themore »
- Authors:
-
- Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1242038
- Grant/Contract Number:
- FG02-91ER20021
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; BolA; cellularmorphology; complementary chromatic acclimation(CCA); cyanobacteria; light signaling; photomorphogenesis
Citation Formats
Singh, Shailendra P., and Montgomery, Beronda L. Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon. United States: N. p., 2015.
Web. doi:10.3389/fmicb.2015.01215.
Singh, Shailendra P., & Montgomery, Beronda L. Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon. United States. https://doi.org/10.3389/fmicb.2015.01215
Singh, Shailendra P., and Montgomery, Beronda L. Thu .
"Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon". United States. https://doi.org/10.3389/fmicb.2015.01215. https://www.osti.gov/servlets/purl/1242038.
@article{osti_1242038,
title = {Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon},
author = {Singh, Shailendra P. and Montgomery, Beronda L.},
abstractNote = {Filamentous cyanobacterium Fremyella diplosiphon is known to alter its pigmentation and morphology during complementary chromatic acclimation (CCA) to efficiently harvest available radiant energy for photosynthesis. F. diplosiphon cells are rectangular and filaments are longer under green light (GL), whereas smaller, spherical cells and short filaments are prevalent under red light (RL). Light regulation of bolA morphogene expression is correlated with photoregulation of cellular morphology in F. diplosiphon. Here, we investigate a role for quantitative regulation of cellular BolA protein levels in morphology determination. Overexpression of bolA in WT was associated with induction of RL-characteristic spherical morphology even when cultures were grown under GL. Overexpression of bolA in a ΔrcaE background, which lacks cyanobacteriochrome photosensor RcaE and accumulates lower levels of BolA than WT, partially reverted the cellular morphology of the strain to a WT-like state. Overexpression of BolA in WT and ΔrcaE backgrounds was associated with decreased cellular reactive oxygen species (ROS) levels and an increase in filament length under both GL and RL. Morphological defects and high ROS levels commonly observed in ΔrcaE could, thus, be in part due to low accumulation of BolA. Together, these findings support an emerging model for RcaE-dependent photoregulation of BolA in controlling the cellular morphology of F. diplosiphon during CCA.},
doi = {10.3389/fmicb.2015.01215},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Thu Nov 05 00:00:00 EST 2015},
month = {Thu Nov 05 00:00:00 EST 2015}
}
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Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis
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Overexpression of FurA in Anabaena sp. PCC 7120 Reveals New Targets for This Regulator Involved in Photosynthesis, Iron Uptake and Cellular Morphology
journal, October 2010
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Responding to Color: The Regulation of Complementary Chromatic Adaptation
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Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
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The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth
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Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin
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Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix
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Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli.
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The phycobilisomes: an early requisite for efficient photosynthesis in cyanobacteria
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Temporal dynamics of changes in reactive oxygen species (ROS) levels and cellular morphology are coordinated during complementary chromatic acclimation in Fremyella diplosiphon
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The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes
journal, October 2007
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New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system.
journal, June 1997
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BolA Inhibits Cell Elongation and Regulates MreB Expression Levels
journal, February 2009
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Complementary Chromatic Adaptation in a Filamentous Blue-Green alga
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Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in F remyella diplosiphon : Photoregulation of morphogenes mediates cell shape
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Independence and interdependence of the photoregulation of pigmentation and development in Fremyella diplosiphon
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Monothiol Glutaredoxin–BolA Interactions: Redox Control of Arabidopsis thaliana BolA2 and SufE1
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- Molecular Plant, Vol. 7, Issue 1
Exploiting the Autofluorescent Properties of Photosynthetic Pigments for Analysis of Pigmentation and Morphology in Live Fremyella diplosiphon Cells
journal, July 2010
- Bordowitz, Juliana R.; Montgomery, Beronda L.
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A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis.
journal, February 1997
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- Journal of Bacteriology, Vol. 179, Issue 4
Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light-responsive promoters: Transcriptional regulation of chromatic adaptation
journal, March 2008
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Phycobiliproteins and Complementary Chromatic Adaptation
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- Annual Review of Plant Physiology, Vol. 26, Issue 1
Light Quantity Affects the Regulation of Cell Shape in Fremyella diplosiphon
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The biological roles of glutaredoxins
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Regulation of biofilm formation and cellular buoyancy through modulating intracellular cyclic di-GMP levels in engineered cyanobacteria: Engineering c-di-GMP Levels in Cyanobacteria
journal, October 2015
- Agostoni, Marco; Waters, Christopher M.; Montgomery, Beronda L.
- Biotechnology and Bioengineering, Vol. 113, Issue 2
Reactive oxygen species are involved in the morphology-determining mechanism of Fremyella diplosiphon cells during complementary chromatic adaptation
journal, June 2012
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Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937
journal, July 2010
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Light intensity and reactive oxygen species are centrally involved in photoregulatory responses during complementary chromatic adaptation in Fremyella diplosiphon
journal, September 2013
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- Communicative & Integrative Biology, Vol. 6, Issue 5
The phycobilisomes: an early requisite for efficient photosynthesis in cyanobacteria
text, January 2015
- Singh, Niraj Kumar; Sonani, Ravi Raghav; Rastogi, Rajesh Prasad
- Technische Universität Dortmund
N2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance
journal, October 2001
- Postius, Christine; Neuschaefer-Rube, Olaf; Haid, Volker
- FEMS Microbiology Ecology, Vol. 37, Issue 2
Emerging Perspectives on the Mechanisms, Regulation, and Distribution of Light Color Acclimation in Cyanobacteria
journal, January 2012
- Gutu, Andrian; Kehoe, David M.
- Molecular Plant, Vol. 5, Issue 1
The Coevolution of Phycobilisomes: Molecular Structure Adapting to Functional Evolution
journal, January 2011
- Shi, Fei; Qin, Song; Wang, Yin-Chu
- Comparative and Functional Genomics, Vol. 2011
Changes in Accumulation and Synthesis of Transcripts Encoding Phycobilisome Components during Acclimation of Fremyella diplosiphon to Different Light Qualities
journal, December 1988
- Oelmüller, R.; Conley, P. B.; Federspiel, N.
- Plant Physiology, Vol. 88, Issue 4
Independence and interdependence of the photoregulation of pigmentation and development in Fremyella diplosiphon
journal, March 2010
- Bordowitz, Juliana R.; Whitaker, Melissa J.; Montgomery, Beronda L.
- Communicative & Integrative Biology, Vol. 3, Issue 2
Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle
journal, March 2013
- Hirose, Y.; Rockwell, N. C.; Nishiyama, K.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 13
Construction of Shuttle Plasmids Which Can Be Efficiently Mobilized from Escherichia coli into the Chromatically Adapting Cyanobacterium, Fremyella diplosiphon
journal, September 1993
- Cobley, John G.; Zerweck, Edward; Reyes, Richard
- Plasmid, Vol. 30, Issue 2
A BolA-like morphogene from the alga Chlamydomonas reinhardtii changes morphology and induces biofilm formation in Escherichia coli
journal, December 2012
- Khona, Dolly K.; Dongre, Shounak S.; Arraiano, Cecilia M.
- FEMS Microbiology Letters, Vol. 339, Issue 1
Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix
journal, May 1996
- Campbell, D.
- Microbiology, Vol. 142, Issue 5
Photoregulation of morphological structure and its physiological relevance in the cyanobacterium Arthrospira (Spirulina) platensis
journal, May 2009
- Ma, Zengling; Gao, Kunshan
- Planta, Vol. 230, Issue 2
The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes
journal, October 2007
- Divakaruni, Arun V.; Baida, Cyril; White, Courtney L.
- Molecular Microbiology, Vol. 66, Issue 1
The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex: MreBCD proteins form an essential membrane complex
journal, October 2004
- Kruse, Thomas; Bork-Jensen, Jette; Gerdes, Kenn
- Molecular Microbiology, Vol. 55, Issue 1
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
journal, March 1968
- Allen, Mary Mennes
- Journal of Phycology, Vol. 4, Issue 1
The phycobilisomes: an early requisite for efficient photosynthesis in cyanobacteria
text, January 2015
- Singh, Niraj Kumar; Sonani, Ravi Raghav; Rastogi, Rajesh Prasad
- Leibniz Research Centre for Working Environment and Human Factors, Dortmund
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Works referencing / citing this record:
RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon
journal, January 2018
- Rohnke, Brandon A.; Singh, Shailendra P.; Pattanaik, Bagmi
- mSphere, Vol. 3, Issue 1
RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon
journal, January 2018
- Rohnke, Brandon A.; Singh, Shailendra P.; Pattanaik, Bagmi
- mSphere, Vol. 3, Issue 1