Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli

ABSTRACT During stationary phase in Escherichia coli, the expression of the ribosome modulation factor (RMF) protein participates in the dimerization of two 70S ribosomes, ultimately creating a 100S particle. 100S ribosomes are commonly thought to function to preserve ribosomes as growth ceases and...

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Main Authors: Hans Sebastian, Steven E. Finkel
Format: Article
Language:English
Published: American Society for Microbiology 2022-04-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02239-21
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author Hans Sebastian
Steven E. Finkel
author_facet Hans Sebastian
Steven E. Finkel
author_sort Hans Sebastian
collection DOAJ
description ABSTRACT During stationary phase in Escherichia coli, the expression of the ribosome modulation factor (RMF) protein participates in the dimerization of two 70S ribosomes, ultimately creating a 100S particle. 100S ribosomes are commonly thought to function to preserve ribosomes as growth ceases and cells begin to catabolize intracellular components, including proteins, during their transition into stationary phase. Here, we show that the rates of stationary-phase ribosomal degradation are increased in an rmf mutant strain that cannot produce 100S ribosomes, resulting in deficiencies in outgrowth upon reinoculation into fresh medium. Upon coinoculation in LB medium, the mutant exhibits a delay in entry into log phase, differences in growth rates, and an overall reduction in relative fitness during competition. Unexpectedly, the rmf mutant exhibited shorter generation times than wild-type cells during log phase, both in monoculture and during competition. These doubling times of ∼13 min suggest that failure to maintain ribosomal balance affects the control of cell division. Though the timing of entry into and exit from log phase is altered, 100S ribosomes are not essential for long-term viability of the rmf mutant when grown in monoculture. IMPORTANCE Ribosomes are the sole source in any cell for new protein synthesis that is vital to maintain life. While ribosomes are frequently consumed as sources of nutrients under low-nutrient conditions, some ribosomes appear to be preserved for later use. The failure to maintain the availability of these ribosomes can lead to a dire consequence upon the influx of new nutrients, as cells are unable to efficiently replenish their metabolic machinery. It is important to study the repercussions, consequences, and mechanisms of survival in cells that cannot properly maintain the availability of their ribosomes in order to better understand their mechanisms of survival during competition under nutrient-depleted conditions.
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spelling doaj.art-86a230b2fc9245c0b80113c72583aa942022-12-22T02:55:38ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-04-0110210.1128/spectrum.02239-21Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coliHans Sebastian0Steven E. Finkel1Molecular and Computational Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, California, USAMolecular and Computational Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, California, USAABSTRACT During stationary phase in Escherichia coli, the expression of the ribosome modulation factor (RMF) protein participates in the dimerization of two 70S ribosomes, ultimately creating a 100S particle. 100S ribosomes are commonly thought to function to preserve ribosomes as growth ceases and cells begin to catabolize intracellular components, including proteins, during their transition into stationary phase. Here, we show that the rates of stationary-phase ribosomal degradation are increased in an rmf mutant strain that cannot produce 100S ribosomes, resulting in deficiencies in outgrowth upon reinoculation into fresh medium. Upon coinoculation in LB medium, the mutant exhibits a delay in entry into log phase, differences in growth rates, and an overall reduction in relative fitness during competition. Unexpectedly, the rmf mutant exhibited shorter generation times than wild-type cells during log phase, both in monoculture and during competition. These doubling times of ∼13 min suggest that failure to maintain ribosomal balance affects the control of cell division. Though the timing of entry into and exit from log phase is altered, 100S ribosomes are not essential for long-term viability of the rmf mutant when grown in monoculture. IMPORTANCE Ribosomes are the sole source in any cell for new protein synthesis that is vital to maintain life. While ribosomes are frequently consumed as sources of nutrients under low-nutrient conditions, some ribosomes appear to be preserved for later use. The failure to maintain the availability of these ribosomes can lead to a dire consequence upon the influx of new nutrients, as cells are unable to efficiently replenish their metabolic machinery. It is important to study the repercussions, consequences, and mechanisms of survival in cells that cannot properly maintain the availability of their ribosomes in order to better understand their mechanisms of survival during competition under nutrient-depleted conditions.https://journals.asm.org/doi/10.1128/spectrum.02239-21100S ribosomecompetitive fitnesslong-term survivalribosome modulating factor
spellingShingle Hans Sebastian
Steven E. Finkel
Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli
Microbiology Spectrum
100S ribosome
competitive fitness
long-term survival
ribosome modulating factor
title Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli
title_full Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli
title_fullStr Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli
title_full_unstemmed Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli
title_short Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli
title_sort absence of ribosome modulation factor alters growth and competitive fitness of escherichia coli
topic 100S ribosome
competitive fitness
long-term survival
ribosome modulating factor
url https://journals.asm.org/doi/10.1128/spectrum.02239-21
work_keys_str_mv AT hanssebastian absenceofribosomemodulationfactoraltersgrowthandcompetitivefitnessofescherichiacoli
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