Evolution of pH- sensitive transcription termination in Escherichia coli during adaptation to repeated long- term starvation

• 成果类型: Article
• 署名作者: Worthan, Sarah B.; McCarthy, Robert D. P.; Delaleau, Mildred; Stikeleather, Ryan; Bratton, Benjamin P.; Boudvillain, Marc; Behringer, Megan G.
• 署名单位: Vanderbilt University; Vanderbilt University; Centre National de la Recherche Scientifique (CNRS); CNRS - Institute of Chemistry (INC); Universite de Orleans; Arizona State University; Arizona State University-Tempe; Vanderbilt University; Vanderbilt University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9734
• DOI: 10.1073/pnas.2405546121
• 发表日期: 2024-09-24
• 关键词: amino-acid catabolism; stationary-phase; fluorescent-probe; growth advantage; intracellular ph; stress-response; factor-rho; histidine; mechanism; mutations

摘要

Fluctuating environments that consist of regular cycles of co- occurring stress are a common challenge faced by cellular populations. For a population to thrive in constantly changing conditions, an ability to coordinate a rapid cellular response is essential. Here, we identify a mutation conferring an arginine-to- histidine (Arg to His) substitution in the transcription terminator Rho. The rho R109H mutation frequently arose in Escherichia coli populations experimentally evolved under repeated long- term starvation conditions, during which the accumulation of metabolic waste followed by transfer into fresh media results in drastic environmental pH fluctuations associated with feast and famine. Metagenomic sequencing revealed that populations containing the rho mutation also possess putative loss- of- function mutations in ydcI, which encodes a recently characterized transcription factor associated with pH homeostasis. Genetic reconstructions of these mutations show that the rho allele confers plasticity via an alkaline- induced reduction of Rho function that, when found in tandem with a Delta ydcI allele, leads to intracellular alkalization and genetic assimilation of Rho mutant function. We further identify Arg to His substitutions at analogous sites in rho alleles from species that regularly experience neutral to alkaline pH fluctuations in their environments. Our results suggest that Arg to His substitutions in Rho may serve to rapidly coordinate complex physiological responses through pH sensing and shed light on how cellular populations use environmental cues to coordinate rapid responses to complex, fluctuating environments.