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Nanocalorimetry Reveals the Growth Dynamics of Escherichia coli Cells Undergoing Adaptive Evolution during Long-Term Stationary Phase.

Authors
  • Robador, Alberto1, 2, 3
  • Amend, Jan P4, 2, 5
  • Finkel, Steven E4, 3
  • 1 Center for Dark Energy Biosphere Investigations (C-DEBI), University of Southern California, Los Angeles, California, USA [email protected]
  • 2 Marine and Environmental Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, California, USA.
  • 3 Molecular and Computational Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, California, USA.
  • 4 Center for Dark Energy Biosphere Investigations (C-DEBI), University of Southern California, Los Angeles, California, USA.
  • 5 Department of Earth Sciences, University of Southern California, Los Angeles, California, USA.
Type
Published Article
Journal
Applied and Environmental Microbiology
Publisher
American Society for Microbiology
Publication Date
Aug 01, 2019
Volume
85
Issue
15
Identifiers
DOI: 10.1128/AEM.00968-19
PMID: 31152016
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

Bacterial populations in long-term stationary-phase (LTSP) laboratory cultures can provide insights into physiological and genetic adaptations to low-energy conditions and population dynamics in natural environments. While overall population density remains stable, these communities are very dynamic and are characterized by the rapid emergence and succession of distinct mutants expressing the growth advantage in stationary phase (GASP) phenotype, which can reflect an increased capacity to withstand energy limitations and environmental stress. Here, we characterize the metabolic heat signatures and growth dynamics of GASP mutants within an evolving population using isothermal calorimetry. We aged Escherichia coli in anaerobic batch cultures over 20 days inside an isothermal nanocalorimeter and observed distinct heat events related to the emergence of three mutant populations expressing the GASP phenotype after 1.5, 3, and 7 days. Given the heat produced by each population, the maximum number of GASP mutant cells was calculated, revealing abundances of ∼2.5 × 107, ∼7.5 × 106, and ∼9.9 × 106 cells in the populations, respectively. These data indicate that mutants capable of expressing the GASP phenotype can be acquired during the exponential growth phase and subsequently expressed in LTSP culture.IMPORTANCE The present study is innovative in that we have identified previously unknown growth dynamics related to the temporal expression of the growth advantage in stationary phase (GASP) phenotype that allow mutants in long-term stationary-phase cultures to capitalize on the decrease of energy over prolonged incubation periods. By remaining in an active, but growth-limited, metabolic state similar to that observed in GASP cells grown in vitro, natural microbial communities might be able to prevail over much longer time scales. We believe this report to be a remarkable methodological and conceptual breakthrough in the study of the long-term survival and evolution of bacteria. Copyright © 2019 American Society for Microbiology.

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