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Title: Exploiting rRNA operon copy number to investigate bacterial reproductive strategies

Abstract

The potential for rapid reproduction is a hallmark of microbial life, but microbes in nature must also survive and compete when growth is constrained by resource availability. Successful reproduction requires different strategies when resources are scarce and when they are abundant but a systematic framework for predicting these reproductive strategies in bacteria has not been available. Here, we show that the number of ribosomal RNA operons (rrn) in bacterial genomes predicts two important components of reproduction—growth rate and growth efficiency—which are favoured under contrasting regimes of resource availability. We find that the maximum reproductive rate of bacteria doubles with a doubling of rrn copy number, and the efficiency of carbon use is inversely related to maximal growth rate and rrn copy number. We also identify a feasible explanation for these patterns: the rate and yield of protein synthesis mirror the overall pattern in maximum growth rate and growth efficiency. Furthermore, comparative analysis of genomes from 1,167 bacterial species reveals that rrn copy number predicts traits associated with resource availability, including chemotaxis and genome streamlining. Genome-wide patterns of orthologous gene content covary with rrn copy number, suggesting convergent evolution in response to resource availability. Our findings imply that basic cellular processesmore » adapt in contrasting ways to long-term differences in resource availability. They also establish a basis for predicting changes in bacterial community composition in response to resource perturbations using rrn copy number measurements or inferences.« less

Authors:
 [1];  [2];  [2]
  1. Univ. of Michigan, Ann Arbor, MI (United States); Michigan State Univ., East Lansing, MI (United States)
  2. Univ. of Michigan, Ann Arbor, MI (United States)
Publication Date:
Research Org.:
Univ. of Michigan, Ann Arbor, MI (United States)
Sponsoring Org.:
National Science Foundation (NSF); National Institutes of Health (NIH); USDOE
OSTI Identifier:
1418579
Grant/Contract Number:  
AC05-06OR23100; DEB 1027253
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 1; Journal Issue: 11; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Roller, Benjamin R., Stoddard, Steven F., and Schmidt, Thomas M. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. United States: N. p., 2016. Web. doi:10.1038/nmicrobiol.2016.160.
Roller, Benjamin R., Stoddard, Steven F., & Schmidt, Thomas M. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. United States. doi:10.1038/nmicrobiol.2016.160.
Roller, Benjamin R., Stoddard, Steven F., and Schmidt, Thomas M. Mon . "Exploiting rRNA operon copy number to investigate bacterial reproductive strategies". United States. doi:10.1038/nmicrobiol.2016.160. https://www.osti.gov/servlets/purl/1418579.
@article{osti_1418579,
title = {Exploiting rRNA operon copy number to investigate bacterial reproductive strategies},
author = {Roller, Benjamin R. and Stoddard, Steven F. and Schmidt, Thomas M.},
abstractNote = {The potential for rapid reproduction is a hallmark of microbial life, but microbes in nature must also survive and compete when growth is constrained by resource availability. Successful reproduction requires different strategies when resources are scarce and when they are abundant but a systematic framework for predicting these reproductive strategies in bacteria has not been available. Here, we show that the number of ribosomal RNA operons (rrn) in bacterial genomes predicts two important components of reproduction—growth rate and growth efficiency—which are favoured under contrasting regimes of resource availability. We find that the maximum reproductive rate of bacteria doubles with a doubling of rrn copy number, and the efficiency of carbon use is inversely related to maximal growth rate and rrn copy number. We also identify a feasible explanation for these patterns: the rate and yield of protein synthesis mirror the overall pattern in maximum growth rate and growth efficiency. Furthermore, comparative analysis of genomes from 1,167 bacterial species reveals that rrn copy number predicts traits associated with resource availability, including chemotaxis and genome streamlining. Genome-wide patterns of orthologous gene content covary with rrn copy number, suggesting convergent evolution in response to resource availability. Our findings imply that basic cellular processes adapt in contrasting ways to long-term differences in resource availability. They also establish a basis for predicting changes in bacterial community composition in response to resource perturbations using rrn copy number measurements or inferences.},
doi = {10.1038/nmicrobiol.2016.160},
journal = {Nature Microbiology},
number = 11,
volume = 1,
place = {United States},
year = {2016},
month = {9}
}

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