Regulation of bacterial stringent response by an evolutionarily conserved ribosomal protein L11 methylation

Walukiewicz, Hanna E.; Farris, Yuliya; Burnet, Meagan C.; Feid, Sarah C.; You, Youngki; Kim, Hyeyoon; Bank, Thomas; Christensen, David; Payne, Samuel H.; Wolfe, Alan J.; Rao, Christopher V.; Nakayasu, Ernesto S.

doi:10.1128/mbio.01773-24

Regulation of bacterial stringent response by an evolutionarily conserved ribosomal protein L11 methylation

Journal Article · Tue Aug 27 00:00:00 EDT 2024 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.01773-24· OSTI ID:2527256

^[1]; Farris, Yuliya ^[2]; Burnet, Meagan C. ^[2]; ^[3]; ^[2]; ^[2]; Bank, Thomas ^[3]; ^[3]; ^[4]; ^[3]; ^[1]; ^[2]

Univ. of Illinois at Urbana-Champaign, IL (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Loyola University Chicago, Maywood, IL (United States)
Brigham Young Univ., Provo, UT (United States)

Lysine and arginine methylation is an important regulator of enzyme activity and transcription in eukaryotes. However, little is known about this covalent modification in bacteria. In this work, we investigated the role of methylation in bacteria. By reanalyzing a large phyloproteomics data set from 48 bacterial strains representing six phyla, we found that almost a quarter of the bacterial proteome is methylated. Many of these methylated proteins are conserved across diverse bacterial lineages, including those involved in central carbon metabolism and translation. Among the proteins with the most conserved methylation sites is ribosomal protein L11 (bL11). bL11 methylation has been a mystery for five decades, as the deletion of its methyltransferase PrmA causes no cell growth defects. Comparative proteomics analysis combined with inorganic polyphosphate and guanosine tetra/pentaphosphate assays of the ΔprmA mutant in Escherichia coli revealed that bL11 methylation is important for stringent response signaling. In the stationary phase, we found that the ΔprmA mutant has impaired guanosine tetra/pentaphosphate production. This leads to a reduction in inorganic polyphosphate levels, accumulation of RNA and ribosomal proteins, and an abnormal polysome profile. Overall, our investigation demonstrates that the evolutionarily conserved bL11 methylation is important for stringent response signaling and ribosomal activity regulation and turnover.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

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

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2527256

Report Number(s):: PNNL-SA--186921

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 10 Vol. 15; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
arginine methylation
evolutionarily conservation
lysine methylation
phyloproteomics
post-translational modification
starvation
stringent response

Regulation of bacterial stringent response by an evolutionarily conserved ribosomal protein L11 methylation

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