The Role of Two-Component Regulation Systems in the physiology of the Bacterial Cell

Martijn Bekker; M Joost Teixeira De Mattos; Klaas J Hellingwerf

doi:10.3184/003685006783238308

. 2019 Feb 27;89(3-4):213–242. doi: 10.3184/003685006783238308

The Role of Two-Component Regulation Systems in the physiology of the Bacterial Cell

Martijn Bekker ³, M Joost Teixeira De Mattos ², Klaas J Hellingwerf ^1,^✉

¹Laboratory for Microbiology, Swammerdam Institute for Life Sciences, Nieuwe Achtergracht 166, 1018 WV Amsterdam, The Netherlands

²University of Amsterdam, Department of Microbiology of the same university

³University of Amsterdam

^✉

E-mail: K.Hellingwerf@science.uva.nl

He received his masters in chemistry from the University of Groningen, and his PhD in Biochemistry from the University of Amsterdam on “The structure/function relationship of bacteriorhodopsin liposomes”. From 1978 to 1988 he was staff member of the Biology Department of the University of Groningen. Within the Laboratory for Microbiology of this university he studied anoxygenic photosynthesis in Rhodobacter sphaeroides in relation to membrane transport. Since January 1988 he has held the chair in General microbiology at the University of Amsterdam. During this time he has been visiting scientist at the universities of San Diego, Beijing, Buenos Aires and Paris. His research focuses on the molecular basis of signal transduction and the ensuing (stress) response reactions in micro-organisms. Light-activated signal transduction pathways play a roll-model function in his research, because they allow unprecedented temporal and spatial resolution. Since 2004 he has also been honorary professor in the Physics of biological photoreception at the Free University of Amsterdam (VU). He is (co)author of more than 200 peer-reviewed research papers and is member of the board of various local, national and international research organizations.

In 1996, he was appointed Associate Professor at the University of Amsterdam. His main interest within the field of microbiology deals with the adaptive responses of bacterial and yeast species to environmental conditions. He studies these responses by combining quantitative analysis of the activity of metabolic pathways under fully-defined and controlled steady state conditions with time-resolved analyses of these activities upon perturbation of steady state growth. Emphasis is on the adaptive strategies to nutrient-limited environments on the one hand and on the availability of electron acceptors for respiration on the other. Whereas his focus initially was on microbial flux analysis, it now has shifted towards a systems-biological approach in which events at the level of fluxes are integrated with those at the transcriptome and metabolome level.

His thesis project in the Laboratory for Molecular Microbial Physiology at the Swammerdam Institute for Life Sciences of the University of Amsterdam was entitled: “The physiological signals that modulate the activity of the Arc (Aerobic regulation of catabolism) Two-component system”. After developing a method for determination of the redox state of the quinone pools in Escherichia coli, his current research focuses on all aspects of ArcB regulation.

PMCID: PMC10368358 PMID: 17338439

Abstract

Two-component regulation systems (TCRSs) are the dominant type of signal transduction system in prokaryotes that are used to inform the cellular trancriptional machinery (and additional targets for regulation, like the motility apparatus) about actual changes in the extracellular physico-chemical conditions. We now review their molecular structure and enzymatic characteristics, their mutual interactions and its implications, and their role in cellular physiology. Specific emphasis is placed on the ArcB/A system, a representative of the phosphorelay type of TCRS, and a key player in the adjustment of the cellular make-up of enterobacteria in response to alterations in the oxygen availability. Also some applied aspects of the TCRSs are discussed, i.e. their role as a target to develop new anti-bacterials and their application in biotechnology (or: ‘synthetic biology’).

Keywords: Two-component system, TCRS, physiology, histidine protein kinase, response regulator, antimicrobials, signal transduction, synthetic biology, ArcB, oxygen regulation

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References

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[bibr1-003685006783238308] 1.Ulrich L. E., Koonin E. V., and Zhulin I. B. (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol., 13, 52. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr2-003685006783238308] 2.Koretke K. K., Lupas A. N., Warren P. V., Rosenberg M., and Brown J. R. (2000) Evolution of two-component signal transduction. Molec. Biol. Evolut., 17, 1956. [DOI] [PubMed] [Google Scholar]

[bibr3-003685006783238308] 3.Jung K. H., Trivedi V. D., and Spudich J. L. (2003) Demonstration of a sensory rhodopsin in eubacteria. Molec. Microbiol., 47, 1513. [DOI] [PubMed] [Google Scholar]

[bibr4-003685006783238308] 4.Galperin M. Y. (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol., 5, 35. [DOI] [PMC free article] [PubMed] [Google Scholar]

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[bibr6-003685006783238308] 6.Parkinson J. S., and Kofoid E. C. (1992) Communication modules in bacterial signaling proteins. Annu. Rev. Genet., 26, 71. [DOI] [PubMed] [Google Scholar]

[bibr7-003685006783238308] 7.Qin L., Cai S., Zhu Y., and Inouye M. (2003) Cysteine-scanning analysis of the dimerization domain of Env, zan osmosensing histidine kinase. J. Bacteriol., 185, 3429. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr8-003685006783238308] 8.West A. H., and Stock A. M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci., 26, 369. [DOI] [PubMed] [Google Scholar]

[bibr9-003685006783238308] 9.Zapf J., Sen U., Madhusudan, Hoch J. A., and Varughese K. I. (2000) A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure, 8, 851. [DOI] [PubMed] [Google Scholar]

[bibr10-003685006783238308] 10.Xu Q., Porter S. W., and West A. H. (2003) The yeast YPD1/SLN1 complex: insights into molecular recognition in two-component signaling systems. Structure, 11, 1569. [DOI] [PubMed] [Google Scholar]

[bibr11-003685006783238308] 11.Mukhopadhyay D., and Varughese K. I. (2005) A computational analysis on the specificity of interactions between histidine kinases and response regulators. J. Biomolec. Struct. Dyn., 22, 555. [DOI] [PubMed] [Google Scholar]

[bibr12-003685006783238308] 12.Kim D., and Forst S. (2001) Genomic analysis of the histidine kinase family in bacteria and archaea. Microbiology, 147, 1197. [DOI] [PubMed] [Google Scholar]

[bibr13-003685006783238308] 13.Galperin M. Y. (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol., 188, 4169. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr14-003685006783238308] 14.Zhang W., and Shi L. (2005) Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology, 151, 2159. [DOI] [PubMed] [Google Scholar]

[bibr15-003685006783238308] 15.Dutta R., Qin L., and Inouye M. (1999) Histidine kinases: diversity of domain organization. Molec. Microbiol., 34, 633. [DOI] [PubMed] [Google Scholar]

[bibr16-003685006783238308] 16.Hellingwerf K. J. (2005) Bacterial observations: a rudimentary form of intelligence? Trends Microbiol., 13, 152. [DOI] [PubMed] [Google Scholar]

[bibr17-003685006783238308] 17.Yamamoto K., Hirao K., Oshima T., Aiba H., Utsumi R., and Ishihama A. (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem., 280, 1448. [DOI] [PubMed] [Google Scholar]

[bibr18-003685006783238308] 18.Matsubara M., Kitaoka S. L., Takeda S. I., and Mizuno T. (2000) Tuning of the porin expression under anaerobic growth conditions by his-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor in Escherichia coli. Genes Cells, 5, 555. [DOI] [PubMed] [Google Scholar]

[bibr19-003685006783238308] 19.Jacobs C., Hung D., and Shapiro L. (2001) Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc. Natl. Acad. Sci. USA, 98, 4095. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr20-003685006783238308] 20.Kato A., and Groisman E. A. (2004) Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev., 18, 2302. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr21-003685006783238308] 21.Eguchi Y., and Utsumi R. (2005) A novel mechanism for connecting bacterial two-component signal-transduction systems. Trends Biochem. Sci., 30, 70. [DOI] [PubMed] [Google Scholar]

[bibr22-003685006783238308] 22.Oshima T., Aiba H., Masuda Y., Kanaya S., Sugiura M., Wanner B. L., Mori H., and Mizuno T. (2002) Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Molec. Microbiol., 46, 281. [DOI] [PubMed] [Google Scholar]

[bibr23-003685006783238308] 23.Ogura M., Yamaguchi H., Yoshida K., Fujita Y., and Tanaka T. (2001) DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B. subtilis two-component regulatory systems. Nucl. Acids Res., 29, 3804. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr24-003685006783238308] 24.Kobayashi K., Ogura M., Yamaguchi H., Yoshida K., Ogasawara N., Tanaka T., and Fujita Y. (2001) Comprehensive DNA microarray analysis of Bacillus subtilis two-component regulatory systems. J. Bacterio., 183, 7365. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr25-003685006783238308] 25.Hagiwara D., Sugiura M., Oshima T., Mori H., Aiba H., Yamashino T., and Mizuno T. (2003) Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J. Bacteriol., 185, 5735. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr26-003685006783238308] 26.Hagiwara D., Yamashino T., and Mizuno T. (2004) A Genome-wide view of the Escherichia coli BasS-BasR two-component system implicated in iron-responses. Biosci. Biotechnol. Biochem., 68, 1758. [DOI] [PubMed] [Google Scholar]

[bibr27-003685006783238308] 27.Lee L. J., Barrett J. A., and Poole R. K. (2005) Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc. J. Bacteriol., 187, 1124. [DOI] [PMC free article] [PubMed] [Google Scholar]

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The Role of Two-Component Regulation Systems in the physiology of the Bacterial Cell

Martijn Bekker

M Joost Teixeira De Mattos

Klaas J Hellingwerf

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The Role of Two-Component Regulation Systems in the physiology of the Bacterial Cell

Martijn Bekker

M Joost Teixeira De Mattos

Klaas J Hellingwerf

Abstract

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