Dissection of the mutation accumulation process during bacterial range expansions

Abstract Background Recent experimental work has shown that the evolutionary dynamics of bacteria expanding across space can differ dramatically from what we expect under well-mixed conditions. During spatial expansion, deleterious mutations can accumulate due to inefficient selection on the expansi...

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Main Authors: Lars Bosshard, Stephan Peischl, Martin Ackermann, Laurent Excoffier
Format: Article
Language:English
Published: BMC 2020-03-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-6676-z
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spelling doaj-3af57835a852463cb84fe68f1c77a5aa2020-11-25T02:25:04ZengBMCBMC Genomics1471-21642020-03-0121111110.1186/s12864-020-6676-zDissection of the mutation accumulation process during bacterial range expansionsLars Bosshard0Stephan Peischl1Martin Ackermann2Laurent Excoffier3CMPG, Institute of Ecology an Evolution, University of BerneSwiss Institute of BioinformaticsInstitute of Biogeochemistry and Pollutant Dynamics, Swiss Federal Institute of Technology Zurich (ETH Zürich)CMPG, Institute of Ecology an Evolution, University of BerneAbstract Background Recent experimental work has shown that the evolutionary dynamics of bacteria expanding across space can differ dramatically from what we expect under well-mixed conditions. During spatial expansion, deleterious mutations can accumulate due to inefficient selection on the expansion front, potentially interfering with and modifying adaptive evolutionary processes. Results We used whole genome sequencing to follow the genomic evolution of 10 mutator Escherichia coli lines during 39 days ( ~ 1650 generations) of a spatial expansion, which allowed us to gain a temporal perspective on the interaction of adaptive and non-adaptive evolutionary processes during range expansions. We used elastic net regression to infer the positive or negative effects of mutations on colony growth. The colony size, measured after three day of growth, decreased at the end of the experiment in all 10 lines, and mutations accumulated at a nearly constant rate over the whole experiment. We find evidence that beneficial mutations accumulate primarily at an early stage of the experiment, leading to a non-linear change of colony size over time. Indeed, the rate of colony size expansion remains almost constant at the beginning of the experiment and then decreases after ~ 12 days of evolution. We also find that beneficial mutations are enriched in genes encoding transport proteins, and genes coding for the membrane structure, whereas deleterious mutations show no enrichment for any biological process. Conclusions Our experiment shows that beneficial mutations target specific biological functions mostly involved in inter or extra membrane processes, whereas deleterious mutations are randomly distributed over the whole genome. It thus appears that the interaction between genetic drift and the availability or depletion of beneficial mutations determines the change in fitness of bacterial populations during range expansion.http://link.springer.com/article/10.1186/s12864-020-6676-zExperimental evolutionRange expansionMutation load
collection DOAJ
language English
format Article
sources DOAJ
author Lars Bosshard
Stephan Peischl
Martin Ackermann
Laurent Excoffier
spellingShingle Lars Bosshard
Stephan Peischl
Martin Ackermann
Laurent Excoffier
Dissection of the mutation accumulation process during bacterial range expansions
BMC Genomics
Experimental evolution
Range expansion
Mutation load
author_facet Lars Bosshard
Stephan Peischl
Martin Ackermann
Laurent Excoffier
author_sort Lars Bosshard
title Dissection of the mutation accumulation process during bacterial range expansions
title_short Dissection of the mutation accumulation process during bacterial range expansions
title_full Dissection of the mutation accumulation process during bacterial range expansions
title_fullStr Dissection of the mutation accumulation process during bacterial range expansions
title_full_unstemmed Dissection of the mutation accumulation process during bacterial range expansions
title_sort dissection of the mutation accumulation process during bacterial range expansions
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-03-01
description Abstract Background Recent experimental work has shown that the evolutionary dynamics of bacteria expanding across space can differ dramatically from what we expect under well-mixed conditions. During spatial expansion, deleterious mutations can accumulate due to inefficient selection on the expansion front, potentially interfering with and modifying adaptive evolutionary processes. Results We used whole genome sequencing to follow the genomic evolution of 10 mutator Escherichia coli lines during 39 days ( ~ 1650 generations) of a spatial expansion, which allowed us to gain a temporal perspective on the interaction of adaptive and non-adaptive evolutionary processes during range expansions. We used elastic net regression to infer the positive or negative effects of mutations on colony growth. The colony size, measured after three day of growth, decreased at the end of the experiment in all 10 lines, and mutations accumulated at a nearly constant rate over the whole experiment. We find evidence that beneficial mutations accumulate primarily at an early stage of the experiment, leading to a non-linear change of colony size over time. Indeed, the rate of colony size expansion remains almost constant at the beginning of the experiment and then decreases after ~ 12 days of evolution. We also find that beneficial mutations are enriched in genes encoding transport proteins, and genes coding for the membrane structure, whereas deleterious mutations show no enrichment for any biological process. Conclusions Our experiment shows that beneficial mutations target specific biological functions mostly involved in inter or extra membrane processes, whereas deleterious mutations are randomly distributed over the whole genome. It thus appears that the interaction between genetic drift and the availability or depletion of beneficial mutations determines the change in fitness of bacterial populations during range expansion.
topic Experimental evolution
Range expansion
Mutation load
url http://link.springer.com/article/10.1186/s12864-020-6676-z
work_keys_str_mv AT larsbosshard dissectionofthemutationaccumulationprocessduringbacterialrangeexpansions
AT stephanpeischl dissectionofthemutationaccumulationprocessduringbacterialrangeexpansions
AT martinackermann dissectionofthemutationaccumulationprocessduringbacterialrangeexpansions
AT laurentexcoffier dissectionofthemutationaccumulationprocessduringbacterialrangeexpansions
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