Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient

ABSTRACT Many nonsporulating bacterial species can survive for years within exhausted growth media in a state termed long-term stationary phase (LTSP). We have been carrying out evolutionary experiments aimed at elucidating the dynamics of genetic adaptation under LTSP. We showed that Escherichia co...

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Autores principales:	Sarit Avrani, Sophia Katz, Ruth Hershberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	LTSP bacterial evolution long-term stationary phase mutators rapid adaptation soft sweeps Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9b2d296f6e6e468b95539494b33540b8
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spelling	oai:doaj.org-article:9b2d296f6e6e468b95539494b33540b82021-11-15T15:30:50ZAdaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient10.1128/mSphere.00388-202379-5042https://doaj.org/article/9b2d296f6e6e468b95539494b33540b82020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00388-20https://doaj.org/toc/2379-5042ABSTRACT Many nonsporulating bacterial species can survive for years within exhausted growth media in a state termed long-term stationary phase (LTSP). We have been carrying out evolutionary experiments aimed at elucidating the dynamics of genetic adaptation under LTSP. We showed that Escherichia coli adapts to prolonged resource exhaustion through the highly convergent acquisition of mutations. In the most striking example of such convergent adaptation, we observed that across all independently evolving LTSP populations, over 90% of E. coli cells carry mutations to one of three specific sites of the RNA polymerase core enzyme (RNAPC). These LTSP adaptations reduce the ability of the cells carrying them to grow once fresh resources are again provided. Here, we examine how LTSP populations recover from costs associated with their adaptation once resources are again provided to them. We demonstrate that due to the ability of LTSP populations to maintain high levels of standing genetic variation during adaptation, costly adaptations are very rapidly purged from the population once they are provided with fresh resources. We further demonstrate that recovery from costs acquired during adaptation under LTSP occurs more rapidly than would be possible if LTSP adaptations had fixed during the time populations spent under resource exhaustion. Finally, we previously reported that under LTSP, some clones develop a mutator phenotype, greatly increasing their mutation accumulation rates. Here, we show that the mechanisms by which populations recover from costs associated with fixed adaptations may depend on mutator status. IMPORTANCE Many bacterial species can survive for decades under starvation, following the exhaustion of external growth resources. We have previously shown that bacteria genetically adapt under these conditions in a manner that reduces their ability to grow once resources again become available. Here, we study how populations that have been subject to very prolonged resource exhaustion recover from costs associated with their adaptation. We demonstrate that rapid adaptations acquired under prolonged starvation tend to be highly transient, rapidly reducing in frequency once bacteria are no longer starved. Our results shed light on the longer-term consequences of bacterial survival under prolonged starvation. More generally, these results may also be applicable to understanding longer-term consequences of rapid adaptation to additional conditions as well.Sarit AvraniSophia KatzRuth HershbergAmerican Society for MicrobiologyarticleLTSPbacterial evolutionlong-term stationary phasemutatorsrapid adaptationsoft sweepsMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	LTSP bacterial evolution long-term stationary phase mutators rapid adaptation soft sweeps Microbiology QR1-502
spellingShingle	LTSP bacterial evolution long-term stationary phase mutators rapid adaptation soft sweeps Microbiology QR1-502 Sarit Avrani Sophia Katz Ruth Hershberg Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient
description	ABSTRACT Many nonsporulating bacterial species can survive for years within exhausted growth media in a state termed long-term stationary phase (LTSP). We have been carrying out evolutionary experiments aimed at elucidating the dynamics of genetic adaptation under LTSP. We showed that Escherichia coli adapts to prolonged resource exhaustion through the highly convergent acquisition of mutations. In the most striking example of such convergent adaptation, we observed that across all independently evolving LTSP populations, over 90% of E. coli cells carry mutations to one of three specific sites of the RNA polymerase core enzyme (RNAPC). These LTSP adaptations reduce the ability of the cells carrying them to grow once fresh resources are again provided. Here, we examine how LTSP populations recover from costs associated with their adaptation once resources are again provided to them. We demonstrate that due to the ability of LTSP populations to maintain high levels of standing genetic variation during adaptation, costly adaptations are very rapidly purged from the population once they are provided with fresh resources. We further demonstrate that recovery from costs acquired during adaptation under LTSP occurs more rapidly than would be possible if LTSP adaptations had fixed during the time populations spent under resource exhaustion. Finally, we previously reported that under LTSP, some clones develop a mutator phenotype, greatly increasing their mutation accumulation rates. Here, we show that the mechanisms by which populations recover from costs associated with fixed adaptations may depend on mutator status. IMPORTANCE Many bacterial species can survive for decades under starvation, following the exhaustion of external growth resources. We have previously shown that bacteria genetically adapt under these conditions in a manner that reduces their ability to grow once resources again become available. Here, we study how populations that have been subject to very prolonged resource exhaustion recover from costs associated with their adaptation. We demonstrate that rapid adaptations acquired under prolonged starvation tend to be highly transient, rapidly reducing in frequency once bacteria are no longer starved. Our results shed light on the longer-term consequences of bacterial survival under prolonged starvation. More generally, these results may also be applicable to understanding longer-term consequences of rapid adaptation to additional conditions as well.
format	article
author	Sarit Avrani Sophia Katz Ruth Hershberg
author_facet	Sarit Avrani Sophia Katz Ruth Hershberg
author_sort	Sarit Avrani
title	Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient
title_short	Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient
title_full	Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient
title_fullStr	Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient
title_full_unstemmed	Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient
title_sort	adaptations accumulated under prolonged resource exhaustion are highly transient
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/9b2d296f6e6e468b95539494b33540b8
work_keys_str_mv	AT saritavrani adaptationsaccumulatedunderprolongedresourceexhaustionarehighlytransient AT sophiakatz adaptationsaccumulatedunderprolongedresourceexhaustionarehighlytransient AT ruthhershberg adaptationsaccumulatedunderprolongedresourceexhaustionarehighlytransient
_version_	1718427903333498880

Adaptations Accumulated under Prolonged Resource Exhaustion Are Highly Transient

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