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Microbial population dynamics and evolutionary outcomes under extreme energy limitation

Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 pop...

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Autores principales: Shoemaker, William R., Jones, Stuart E., Muscarella, Mario E., Behringer, Megan G., Lehmkuhl, Brent K., Lennon, Jay T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8379937/
https://www.ncbi.nlm.nih.gov/pubmed/34385301
http://dx.doi.org/10.1073/pnas.2101691118
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author Shoemaker, William R.
Jones, Stuart E.
Muscarella, Mario E.
Behringer, Megan G.
Lehmkuhl, Brent K.
Lennon, Jay T.
author_facet Shoemaker, William R.
Jones, Stuart E.
Muscarella, Mario E.
Behringer, Megan G.
Lehmkuhl, Brent K.
Lennon, Jay T.
author_sort Shoemaker, William R.
collection PubMed
description Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 populations in an effectively closed system for 1,000 d. All but one taxon survived prolonged resource scarcity, yielding estimated times to extinction ranging over four orders of magnitude from 10(0) to 10(5) y. Our findings corroborate reports of long-lived bacteria recovered from ancient environmental samples, while providing insight into mechanisms of persistence. As death rates declined over time, lifespan was extended through the scavenging of dead cells. Although reproduction was suppressed in the absence of exogenous resources, populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of purifying selection as well as molecular signals of adaptation. Consistent ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.
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spelling pubmed-83799372021-08-30 Microbial population dynamics and evolutionary outcomes under extreme energy limitation Shoemaker, William R. Jones, Stuart E. Muscarella, Mario E. Behringer, Megan G. Lehmkuhl, Brent K. Lennon, Jay T. Proc Natl Acad Sci U S A Biological Sciences Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 populations in an effectively closed system for 1,000 d. All but one taxon survived prolonged resource scarcity, yielding estimated times to extinction ranging over four orders of magnitude from 10(0) to 10(5) y. Our findings corroborate reports of long-lived bacteria recovered from ancient environmental samples, while providing insight into mechanisms of persistence. As death rates declined over time, lifespan was extended through the scavenging of dead cells. Although reproduction was suppressed in the absence of exogenous resources, populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of purifying selection as well as molecular signals of adaptation. Consistent ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life. National Academy of Sciences 2021-08-17 2021-08-12 /pmc/articles/PMC8379937/ /pubmed/34385301 http://dx.doi.org/10.1073/pnas.2101691118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Shoemaker, William R.
Jones, Stuart E.
Muscarella, Mario E.
Behringer, Megan G.
Lehmkuhl, Brent K.
Lennon, Jay T.
Microbial population dynamics and evolutionary outcomes under extreme energy limitation
title Microbial population dynamics and evolutionary outcomes under extreme energy limitation
title_full Microbial population dynamics and evolutionary outcomes under extreme energy limitation
title_fullStr Microbial population dynamics and evolutionary outcomes under extreme energy limitation
title_full_unstemmed Microbial population dynamics and evolutionary outcomes under extreme energy limitation
title_short Microbial population dynamics and evolutionary outcomes under extreme energy limitation
title_sort microbial population dynamics and evolutionary outcomes under extreme energy limitation
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8379937/
https://www.ncbi.nlm.nih.gov/pubmed/34385301
http://dx.doi.org/10.1073/pnas.2101691118
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