Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in Fremyella diplosiphon: Photoregulation of morphogenes mediates cell shape

Singh, Shailendra P.; Montgomery, Beronda L.

doi:10.1111/mmi.12649

Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in Fremyella diplosiphon: Photoregulation of morphogenes mediates cell shape

Journal Article · Thu May 29 00:00:00 EDT 2014 · Molecular Microbiology

DOI:https://doi.org/10.1111/mmi.12649· OSTI ID:1603483

Singh, Shailendra P. ^[1]; Montgomery, Beronda L. ^[2]

Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Lab.; MSU DOE Plant Research Laboratory
Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Lab.

Photoregulation of pigmentation during complementary chromatic acclimation (CCA) is well studied in Fremyella diplosiphon; however, mechanistic insights into the CCA-associated morphological changes are still emerging. F. diplosiphon cells are rectangular under green light (GL), whereas cells are smaller and spherical under red light (RL). Here, we investigate the role of morphogenes bolA and mreB during CCA using gene expression and gene function analyses. The F. diplosiphon bolA gene is essential as its complete removal from the genome was unsuccessful. Depletion of bolA resulted in slow growth, morphological defects and the accumulation of high levels of reactive oxygen species in a partially segregated ΔbolA strain. Higher expression of bolA was observed under RL and was correlated with lower expression of mreB and mreC genes in wild type. In a ΔrcaE strain that lacks the red-/green-responsive RcaE photoreceptor, the expression of bolA and mre genes was altered under both RL and GL. Observed gene expression relationships suggest that mreB and mreC expression is controlled by RcaE-dependent photoregulation of bolA expression. Expression of F. diplosiphon bolA and mreB homologues in Escherichia coli demonstrated functional conservation of the encoded proteins. Together, these studies establish roles for bolA and mreB in RcaE-dependent regulation of cellular morphology.

Research Organization:: Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Lab.

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF)

DOE Contract Number:: FG02-91ER20021

OSTI ID:: 1603483

Journal Information:: Molecular Microbiology, Journal Name: Molecular Microbiology Journal Issue: 1 Vol. 93; ISSN 0950-382X

Publisher:: Wiley

Country of Publication:: United States

Language:: English

References (67)

Effect of Escherichia coli Morphogene bolA on Biofilms Vieira, H. L. A.; Freire, P.; Arraiano, C. M. Applied and Environmental Microbiology, Vol. 70, Issue 9 https://doi.org/10.1128/AEM.70.9.5682-5684.2004	journal	September 2004
OpenStat Reference Manual Miller, William https://doi.org/10.1007/978-1-4614-5740-4	book	January 2013
Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis Cabeen, Matthew T.; Jacobs-Wagner, Christine The Journal of Cell Biology, Vol. 179, Issue 3 https://doi.org/10.1083/jcb.200708001	journal	October 2007
Overexpression of FurA in Anabaena sp. PCC 7120 Reveals New Targets for This Regulator Involved in Photosynthesis, Iron Uptake and Cellular Morphology González, Andrés; Bes, M. Teresa; Barja, François Plant and Cell Physiology, Vol. 51, Issue 11 https://doi.org/10.1093/pcp/pcq148	journal	October 2010
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates Allen, Mary Mennes Journal of Phycology, Vol. 4, Issue 1 https://doi.org/10.1111/j.1529-8817.1968.tb04667.x	journal	March 1968
Cell shape determination in Escherichia coli Osborn, Mary J.; Rothfield, Lawrence Current Opinion in Microbiology, Vol. 10, Issue 6 https://doi.org/10.1016/j.mib.2007.09.004	journal	December 2007
Transcriptional Analysis of the Escherichia coli mreBCD Genes Responsible for Morphogenesis and Chromosome Segregation Wachi, Masaaki; Osaka, Kazuyoshi; Kohama, Tomoko Bioscience, Biotechnology, and Biochemistry, Vol. 70, Issue 11 https://doi.org/10.1271/bbb.60315	journal	November 2006
Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors Kehoe, D. M.; Grossman, A. R. Science, Vol. 273, Issue 5280 https://doi.org/10.1126/science.273.5280.1409	journal	September 1996
I-TASSER server for protein 3D structure prediction Zhang, Yang BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-40	journal	January 2008
Abundance Changes of the Response Regulator RcaC Require Specific Aspartate and Histidine Residues and Are Necessary for Normal Light Color Responsiveness Li, L.; Kehoe, D. M. Journal of Bacteriology, Vol. 190, Issue 21 https://doi.org/10.1128/JB.00762-08	journal	August 2008
The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex: MreBCD proteins form an essential membrane complex Kruse, Thomas; Bork-Jensen, Jette; Gerdes, Kenn Molecular Microbiology, Vol. 55, Issue 1 https://doi.org/10.1111/j.1365-2958.2004.04367.x	journal	October 2004
Monothiol Glutaredoxin–BolA Interactions: Redox Control of Arabidopsis thaliana BolA2 and SufE1 Couturier, Jérémy; Wu, Hui-Chen; Dhalleine, Tiphaine Molecular Plant, Vol. 7, Issue 1 https://doi.org/10.1093/mp/sst156	journal	January 2014
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Bacterial morphology: why have different shapes? Young, Kevin D. Current Opinion in Microbiology, Vol. 10, Issue 6 https://doi.org/10.1016/j.mib.2007.09.009	journal	December 2007
BolA Affects Cell Growth, and Binds to the Promoters of Penicillin-Binding Proteins 5 and 6 and Regulates Their Expression Guinote, Inês B.; Matos, Rute G.; Freire, Patrick Journal of Microbiology and Biotechnology, Vol. 21, Issue 3 https://doi.org/10.4014/jmb.1009.09034	journal	March 2011
RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness: Characterization of the RcaE photoreceptor Terauchi, Kazuki; Montgomery, Beronda L.; Grossman, Arthur R. Molecular Microbiology, Vol. 51, Issue 2 https://doi.org/10.1046/j.1365-2958.2003.03853.x	journal	January 2004
Functional Characterization of a Cyanobacterial OmpR/PhoB Class Transcription Factor Binding Site Controlling Light Color Responses Bezy, R. P.; Kehoe, D. M. Journal of Bacteriology, Vol. 192, Issue 22 https://doi.org/10.1128/JB.00602-10	journal	September 2010
A BolA-like morphogene from the alga Chlamydomonas reinhardtii changes morphology and induces biofilm formation in Escherichia coli Khona, Dolly K.; Dongre, Shounak S.; Arraiano, Cecilia M. FEMS Microbiology Letters, Vol. 339, Issue 1 https://doi.org/10.1111/1574-6968.12051	journal	December 2012
Emerging Perspectives on the Mechanisms, Regulation, and Distribution of Light Color Acclimation in Cyanobacteria Gutu, Andrian; Kehoe, David M. Molecular Plant, Vol. 5, Issue 1 https://doi.org/10.1093/mp/ssr054	journal	January 2012
FdTonB is involved in the photoregulation of cellular morphology during complementary chromatic adaptation in Fremyella diplosiphon Pattanaik, B.; Montgomery, B. L. Microbiology, Vol. 156, Issue 3 https://doi.org/10.1099/mic.0.035410-0	journal	December 2009
Orchestrating bacterial cell morphogenesis Carballido-Lopez, Rut Molecular Microbiology, Vol. 60, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05161.x	journal	May 2006
SAD phasing using iodide ions in a high-throughput structural genomics environment Abendroth, Jan; Gardberg, Anna S.; Robinson, John I. Journal of Structural and Functional Genomics, Vol. 12, Issue 2 https://doi.org/10.1007/s10969-011-9101-7	journal	February 2011
Reactive oxygen species are involved in the morphology-determining mechanism of Fremyella diplosiphon cells during complementary chromatic adaptation Singh, S. P.; Montgomery, B. L. Microbiology, Vol. 158, Issue Pt_9 https://doi.org/10.1099/mic.0.060475-0	journal	June 2012
New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. Kehoe, D. M.; Grossman, A. R. Journal of Bacteriology, Vol. 179, Issue 12 https://doi.org/10.1128/jb.179.12.3914-3921.1997	journal	June 1997
Characterization of the BolA Homolog IbaG: A New Gene Involved in Acid Resistance Guinote, Ines Batista Journal of Microbiology and Biotechnology, Vol. 22, Issue 4 https://doi.org/10.4014/jmb.1107.07037	journal	April 2012
Genomic DNA Microarray Analysis: Identification of New Genes Regulated by Light Color in the Cyanobacterium Fremyella diplosiphon Stowe-Evans, E. L.; Ford, J.; Kehoe, D. M. Journal of Bacteriology, Vol. 186, Issue 13 https://doi.org/10.1128/JB.186.13.4338-4349.2004	journal	June 2004
MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120: Chromosome partitioning in a cyanobacterium Hu, Bin; Yang, Guohua; Zhao, Weixing Molecular Microbiology, Vol. 63, Issue 6 https://doi.org/10.1111/j.1365-2958.2007.05618.x	journal	January 2007
Protein structure prediction on the Web: a case study using the Phyre server Kelley, Lawrence A.; Sternberg, Michael J. E. Nature Protocols, Vol. 4, Issue 3 https://doi.org/10.1038/nprot.2009.2	journal	February 2009
The biological roles of glutaredoxins Ströher, Elke; Millar, A. Harvey Biochemical Journal, Vol. 446, Issue 3 https://doi.org/10.1042/BJ20112131	journal	August 2012
The Selective Value of Bacterial Shape Young, K. D. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 3 https://doi.org/10.1128/MMBR.00001-06	journal	September 2006
BOLA1 Is an Aerobic Protein That Prevents Mitochondrial Morphology Changes Induced by Glutathione Depletion Willems, Peter; Wanschers, Bas F. J.; Esseling, John Antioxidants & Redox Signaling, Vol. 18, Issue 2 https://doi.org/10.1089/ars.2011.4253	journal	January 2013
Distinct salt-dependent effects impair Fremyella diplosiphon pigmentation and cellular shape Singh, Shailendra P.; Montgomery, Beronda L. Plant Signaling & Behavior, Vol. 8, Issue 7 https://doi.org/10.4161/psb.24713	journal	July 2013
Analysis of rpoS and bolA gene expression under various stress-induced environments in planktonic and biofilm phase using 2−ΔΔCT method Adnan, Mohd; Morton, Glyn; Hadi, Sibte Molecular and Cellular Biochemistry, Vol. 357, Issue 1-2 https://doi.org/10.1007/s11010-011-0898-y	journal	June 2011
Solution structure of a BolA-like protein from Mus musculus Kasai, T. Protein Science, Vol. 13, Issue 2 https://doi.org/10.1110/ps.03401004	journal	February 2004
The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes Divakaruni, Arun V.; Baida, Cyril; White, Courtney L. Molecular Microbiology, Vol. 66, Issue 1 https://doi.org/10.1111/j.1365-2958.2007.05910.x	journal	October 2007
Light Quantity Affects the Regulation of Cell Shape in Fremyella diplosiphon Pattanaik, Bagmi; Whitaker, Melissa J.; Montgomery, Beronda L. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00170	journal	January 2012
Construction of Shuttle Plasmids Which Can Be Efficiently Mobilized from Escherichia coli into the Chromatically Adapting Cyanobacterium, Fremyella diplosiphon Cobley, John G.; Zerweck, Edward; Reyes, Richard Plasmid, Vol. 30, Issue 2 https://doi.org/10.1006/plas.1993.1037	journal	September 1993
A Turquoise Mutant Genetically Separates Expression of Genes Encoding Phycoerythrin and Its Associated Linker Peptides Seib, L. O.; Kehoe, D. M. Journal of Bacteriology, Vol. 184, Issue 4 https://doi.org/10.1128/jb.184.4.962-970.2002	journal	February 2002
Sublethal High Hydrostatic Pressure Treatment Reveals the Importance of Genes Coding Cytoskeletal Protein in Escherichia Coli Morphogenesis Abe, Atsumu; Furukawa, Soichi; Migita, Yuya Current Microbiology, Vol. 67, Issue 5 https://doi.org/10.1007/s00284-013-0392-8	journal	May 2013
Shedding new light on the regulation of complementary chromatic adaptation Montgomery, Beronda Open Life Sciences, Vol. 3, Issue 4 https://doi.org/10.2478/s11535-008-0039-0	journal	January 2008
Multidimensional View of the Bacterial Cytoskeleton Celler, K.; Koning, R. I.; Koster, A. J. Journal of Bacteriology, Vol. 195, Issue 8 https://doi.org/10.1128/JB.02194-12	journal	February 2013
Temporal responses of wild-type pigmentation and RcaE-deficient strains of Fremyella diplosiphon during light transitions Singh, Shailendra P.; Montgomery, Beronda L. Communicative & Integrative Biology, Vol. 4, Issue 5 https://doi.org/10.4161/cib.16788	journal	September 2011
Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin Huynen, Martijn A.; Spronk, Chris A. E. M.; Gabaldón, Toni FEBS Letters, Vol. 579, Issue 3 https://doi.org/10.1016/j.febslet.2004.11.111	journal	December 2004
Determining cell shape: adaptive regulation of cyanobacterial cellular differentiation and morphology Singh, Shailendra P.; Montgomery, Beronda L. Trends in Microbiology, Vol. 19, Issue 6 https://doi.org/10.1016/j.tim.2011.03.001	journal	June 2011
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
N2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance Postius, Christine; Neuschaefer-Rube, Olaf; Haid, Volker FEMS Microbiology Ecology, Vol. 37, Issue 2 https://doi.org/10.1111/j.1574-6941.2001.tb00859.x	journal	October 2001
A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis. Kahn, K.; Mazel, D.; Houmard, J. Journal of Bacteriology, Vol. 179, Issue 4 https://doi.org/10.1128/jb.179.4.998-1006.1997	journal	February 1997
Photoregulation of Cellular Morphology during Complementary Chromatic Adaptation Requires Sensor-Kinase-Class Protein RcaE in Fremyella diplosiphon Bordowitz, J. R.; Montgomery, B. L. Journal of Bacteriology, Vol. 190, Issue 11 https://doi.org/10.1128/JB.00018-08	journal	April 2008
Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD: Control of cell shape in bacteria White, Courtney L.; Kitich, Aleksandar; Gober, James W. Molecular Microbiology, Vol. 76, Issue 3 https://doi.org/10.1111/j.1365-2958.2010.07108.x	journal	March 2010
Bacterial Shape: Two-Dimensional Questions and Possibilities Young, Kevin D. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.112408.134102	journal	October 2010
Protein-DNA Recognition Pabo, C. O.; Sauer, R. T. Annual Review of Biochemistry, Vol. 53, Issue 1 https://doi.org/10.1146/annurev.bi.53.070184.001453	journal	June 1984
Induction of a growth-phase-dependent promoter triggers transcription of bolA, an Escherichia coli morphogene. Aldea, M.; Garrido, T.; Hernández-Chico, C. The EMBO Journal, Vol. 8, Issue 12 https://doi.org/10.1002/j.1460-2075.1989.tb08573.x	journal	December 1989
Letter to the Editor: NMR structure note ? Solution structure of a bacterial BolA-like protein XC975 from a plant pathogen Xanthomonas campestris pv. campestris Chin, Ko-Hsin; Lin, Fu-Yang; Hu, Yu-Chen Journal of Biomolecular NMR, Vol. 31, Issue 2 https://doi.org/10.1007/s10858-004-7804-9	journal	February 2005
Global Gene Expression Patterns of Nostoc punctiforme in Steady-State Dinitrogen-Grown Heterocyst-Containing Cultures and at Single Time Points during the Differentiation of Akinetes and Hormogonia Campbell, E. L.; Summers, M. L.; Christman, H. Journal of Bacteriology, Vol. 189, Issue 14 https://doi.org/10.1128/JB.00360-07	journal	May 2007
Exploiting the Autofluorescent Properties of Photosynthetic Pigments for Analysis of Pigmentation and Morphology in Live Fremyella diplosiphon Cells Bordowitz, Juliana R.; Montgomery, Beronda L. Sensors, Vol. 10, Issue 7 https://doi.org/10.3390/s100706969	journal	July 2010
Comparative proteomics of cell division mutants and wild-type of Synechococcus sp. strain PCC 7942 Koksharova, O. A.; Klint, J.; Rasmussen, U. Microbiology, Vol. 153, Issue 8 https://doi.org/10.1099/mic.0.2007/007039-0	journal	August 2007
The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments Bustin, S. A.; Benes, V.; Garson, J. A. Clinical Chemistry, Vol. 55, Issue 4 https://doi.org/10.1373/clinchem.2008.112797	journal	February 2009
Light intensity and reactive oxygen species are centrally involved in photoregulatory responses during complementary chromatic adaptation in Fremyella diplosiphon Walters, Kenneth J.; Whitaker, Melissa J.; Singh, Shailendra P. Communicative & Integrative Biology, Vol. 6, Issue 5 https://doi.org/10.4161/cib.25005	journal	September 2013
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Complementary Chromatic Adaptation in a Filamentous Blue-Green alga Bennett, A. The Journal of Cell Biology, Vol. 58, Issue 2 https://doi.org/10.1083/jcb.58.2.419	journal	August 1973
Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis O'Toole, George A.; Kolter, Roberto Molecular Microbiology, Vol. 28, Issue 3 https://doi.org/10.1046/j.1365-2958.1998.00797.x	journal	April 1998
The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth Santos, Jorge M.; Freire, Patrick; Vicente, Miguel Molecular Microbiology, Vol. 32, Issue 4 https://doi.org/10.1046/j.1365-2958.1999.01397.x	journal	May 1999
Contribution of rpoS and bolA genes in biofilm formation in Escherichia coli K-12 MG1655 Adnan, Mohd; Morton, Glyn; Singh, Jaipaul Molecular and Cellular Biochemistry, Vol. 342, Issue 1-2 https://doi.org/10.1007/s11010-010-0485-7	journal	May 2010
BolA Inhibits Cell Elongation and Regulates MreB Expression Levels Freire, Patrick; Neves Moreira, Ricardo; Arraiano, Cecília Maria Journal of Molecular Biology, Vol. 385, Issue 5 https://doi.org/10.1016/j.jmb.2008.12.026	journal	February 2009
Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle Hirose, Y.; Rockwell, N. C.; Nishiyama, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 13 https://doi.org/10.1073/pnas.1302909110	journal	March 2013
Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix Campbell, D. Microbiology, Vol. 142, Issue 5 https://doi.org/10.1099/13500872-142-5-1255	journal	May 1996
Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. Aldea, M.; Hernández-Chico, C.; de la Campa, A. G. Journal of Bacteriology, Vol. 170, Issue 11 https://doi.org/10.1128/jb.170.11.5169-5176.1988	journal	November 1988

Similar Records

Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon

Journal Article · Wed Nov 04 23:00:00 EST 2015 · Frontiers in Microbiology · OSTI ID:1242038

Exploiting the Autofluorescent Properties of Photosynthetic Pigments for Analysis of Pigmentation and Morphology in Live Fremyella diplosiphon Cells

Journal Article · Thu Jul 01 00:00:00 EDT 2010 · Sensors · OSTI ID:1628532

Light Quantity Affects the Regulation of Cell Shape in Fremyella diplosiphon

Journal Article · Sat Dec 31 23:00:00 EST 2011 · Frontiers in Microbiology · OSTI ID:1628062

Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in Fremyella diplosiphon: Photoregulation of morphogenes mediates cell shape

Citation Formats

References (67)

Similar Records

Related Subjects