The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis

Lakey, Bryan D.; Myers, Kevin S.; Alberge, François; Mettert, Erin L.; Kiley, Patricia J.; Noguera, Daniel R.; Donohue, Timothy J.; Crosson, ed., Sean

doi:10.1371/journal.pgen.1010270

The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis

Journal Article · Wed Jun 29 00:00:00 EDT 2022 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1010270· OSTI ID:1875739

; ; ; ; ; ; ; Crosson, ed., Sean

Bacterial two-component systems (TCSs) often function through the detection of an extracytoplasmic stimulus and the transduction of a signal by a transmembrane sensory histidine kinase. This kinase then initiates a series of reversible phosphorylation modifications to regulate the activity of a cognate, cytoplasmic response regulator as a transcription factor. Several TCSs have been implicated in the regulation of cell cycle dynamics, cell envelope integrity, or cell wall development in Escherichia coli and other well-studied Gram-negative model organisms. However, many α-proteobacteria lack homologs to these regulators, so an understanding of how α-proteobacteria orchestrate extracytoplasmic events is lacking. In this work we identify an essential TCS, CenKR ( C ell en velope K inase and R egulator), in the α-proteobacterium Rhodobacter sphaeroides and show that modulation of its activity results in major morphological changes. Using genetic and biochemical approaches, we dissect the requirements for the phosphotransfer event between CenK and CenR, use this information to manipulate the activity of this TCS in vivo , and identify genes that are directly and indirectly controlled by CenKR in Rb . sphaeroides . Combining ChIP-seq and RNA-seq, we show that the CenKR TCS plays a direct role in maintenance of the cell envelope, regulates the expression of subunits of the Tol-Pal outer membrane division complex, and indirectly modulates the expression of peptidoglycan biosynthetic genes. CenKR represents the first TCS reported to directly control the expression of Tol-Pal machinery genes in Gram-negative bacteria, and we predict that homologs of this TCS serve a similar function in other closely related organisms. We propose that Rb . sphaeroides genes of unknown function that are directly regulated by CenKR play unknown roles in cell envelope biosynthesis, assembly, and/or remodeling in this and other α-proteobacteria.

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Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0018409

OSTI ID:: 1875739

Alternate ID(s):: OSTI ID: 1874407

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 6 Vol. 18; ISSN 1553-7404

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

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The role of CenKR in the coordination of Rhodobacter sphaeroides cell elongation and division

Journal Article · Tue Jun 06 20:00:00 EDT 2023 · mBio (Online) · OSTI ID:1984122

The essential Rhodobacter sphaeroides CenKR two-component system regulates cell division and envelope biosynthesis

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