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Title: 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 » cellular morphology of F. diplosiphon during CCA.« less

Authors:
 [1];  [1]
  1. 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. doi:10.3389/fmicb.2015.01215.
Singh, Shailendra P., and Montgomery, Beronda L. Thu . "Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon". United States. doi: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 = {2015},
month = {11}
}

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Works referenced in this record:

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Light intensity and reactive oxygen species are centrally involved in photoregulatory responses during complementary chromatic adaptation in Fremyella diplosiphon
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    Works referencing / citing this record:

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    journal, May 2015

    • Yerrapragada, Shaila; Shukla, Animesh; Hallsworth-Pepin, Kymberlie
    • Genome Announcements, Vol. 3, Issue 3
    • DOI: 10.1128/genomea.00355-15

    N2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance
    journal, October 2001


    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

    • Rastogi, Rajesh P.; Singh, Shailendra P.; Häder, Donat-P.
    • Biochemical and Biophysical Research Communications, Vol. 397, Issue 3
    • DOI: 10.1016/j.bbrc.2010.06.006

    A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis.
    journal, February 1997


    Complementary Chromatic Adaptation in a Filamentous Blue-Green alga
    journal, August 1973


    Functional Characterization of a Cyanobacterial OmpR/PhoB Class Transcription Factor Binding Site Controlling Light Color Responses
    journal, September 2010

    • Bezy, R. P.; Kehoe, D. M.
    • Journal of Bacteriology, Vol. 192, Issue 22
    • DOI: 10.1128/jb.00602-10

    The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex: MreBCD proteins form an essential membrane complex
    journal, October 2004


    Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin
    journal, December 2004


    The biological roles of glutaredoxins
    journal, August 2012

    • Ströher, Elke; Millar, A. Harvey
    • Biochemical Journal, Vol. 446, Issue 3
    • DOI: 10.1042/bj20112131

    Chromatic adaptation and the evolution of light color sensing in cyanobacteria
    journal, May 2010


    RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness: Characterization of the RcaE photoreceptor
    journal, January 2004


    Temporal dynamics of changes in reactive oxygen species (ROS) levels and cellular morphology are coordinated during complementary chromatic acclimation in Fremyella diplosiphon
    journal, October 2013

    • Singh, Shailendra P.; Miller, Haley L.; Montgomery, Beronda L.
    • Photosynthesis Research, Vol. 118, Issue 1-2
    • DOI: 10.1007/s11120-013-9938-7

    BolA Inhibits Cell Elongation and Regulates MreB Expression Levels
    journal, February 2009

    • Freire, Patrick; Neves Moreira, Ricardo; Arraiano, Cecília Maria
    • Journal of Molecular Biology, Vol. 385, Issue 5
    • DOI: 10.1016/j.jmb.2008.12.026

    Responding to Color: The Regulation of Complementary Chromatic Adaptation
    journal, June 2006


    Effect of Escherichia coli Morphogene bolA on Biofilms
    journal, September 2004


    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
    • DOI: 10.1002/bit.25712

    Temporal dynamics of ROS biogenesis under simulated solar radiation in the cyanobacterium Anabaena variabilis PCC 7937
    journal, March 2014


    New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system.
    journal, June 1997


    Structural and Spectroscopic Insights into BolA-Glutaredoxin Complexes
    journal, July 2014

    • Roret, Thomas; Tsan, Pascale; Couturier, Jérémy
    • Journal of Biological Chemistry, Vol. 289, Issue 35
    • DOI: 10.1074/jbc.m114.572701

    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
    • DOI: 10.4161/cib.3.2.10367

    Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis
    journal, October 2007

    • Cabeen, Matthew T.; Jacobs-Wagner, Christine
    • The Journal of Cell Biology, Vol. 179, Issue 3
    • DOI: 10.1083/jcb.200708001

    The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes
    journal, October 2007


    Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors
    journal, September 1996


    Convergence and divergence of the photoregulation of pigmentation and cellular morphology in Fremyella diplosiphon
    journal, December 2011

    • Pattanaik, Bagmi; Whitaker, Melissa J.; Montgomery, Beronda L.
    • Plant Signaling & Behavior, Vol. 6, Issue 12
    • DOI: 10.4161/psb.6.12.18239

    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
    • DOI: 10.1073/pnas.1302909110

    Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli.
    journal, November 1988


    Light Quantity Affects the Regulation of Cell Shape in Fremyella diplosiphon
    journal, January 2012

    • Pattanaik, Bagmi; Whitaker, Melissa J.; Montgomery, Beronda L.
    • Frontiers in Microbiology, Vol. 3
    • DOI: 10.3389/fmicb.2012.00170

    Histidine 103 in Fra2 Is an Iron-Sulfur Cluster Ligand in the [2Fe-2S] Fra2-Grx3 Complex and Is Required for in Vivo Iron Signaling in Yeast
    journal, October 2010

    • Li, Haoran; Mapolelo, Daphne T.; Dingra, Nin N.
    • Journal of Biological Chemistry, Vol. 286, Issue 1
    • DOI: 10.1074/jbc.m110.184176

    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
    • DOI: 10.1155/2011/230236

    Phycobiliproteins and Complementary Chromatic Adaptation
    journal, June 1975


    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

    • González, Andrés; Bes, M. Teresa; Barja, François
    • Plant and Cell Physiology, Vol. 51, Issue 11
    • DOI: 10.1093/pcp/pcq148

    Involvement of reactive oxygen species in the UV-B damage to the cyanobacterium Anabaena sp.
    journal, February 2002


    Breaking through the stress barrier: the role of BolA in Gram-negative survival
    journal, July 2014

    • Guinote, Inês Batista; Moreira, Ricardo Neves; Barahona, Susana
    • World Journal of Microbiology and Biotechnology, Vol. 30, Issue 10
    • DOI: 10.1007/s11274-014-1702-4

    Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
    journal, March 1968


    The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth
    journal, May 1999


    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
    • DOI: 10.1093/mp/ssr054

    Light intensity and reactive oxygen species are centrally involved in photoregulatory responses during complementary chromatic adaptation in Fremyella diplosiphon
    journal, September 2013

    • Walters, Kenneth J.; Whitaker, Melissa J.; Singh, Shailendra P.
    • Communicative & Integrative Biology, Vol. 6, Issue 5
    • DOI: 10.4161/cib.25005

    Monothiol Glutaredoxin–BolA Interactions: Redox Control of Arabidopsis thaliana BolA2 and SufE1
    journal, January 2014

    • Couturier, Jérémy; Wu, Hui-Chen; Dhalleine, Tiphaine
    • Molecular Plant, Vol. 7, Issue 1
    • DOI: 10.1093/mp/sst156

    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
    • DOI: 10.1111/1574-6968.12051