Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations

ABSTRACT Hexavalent chromium [Cr(VI)] is a common environmental pollutant. However, little is known about the genetic basis of microbial evolution under Cr(VI) stress and the influence of the prior evolution histories on the subsequent evolution under Cr(VI) stress. In this study, Desulfovibrio vulg...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Weiling Shi, Qiao Ma, Feiyan Pan, Yupeng Fan, Megan L. Kempher, Daliang Ning, Yuanyuan Qu, Judy D. Wall, Aifen Zhou, Jizhong Zhou
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://doaj.org/article/58d327ded9894b2697bd449653a35e31
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:58d327ded9894b2697bd449653a35e31
record_format dspace
spelling oai:doaj.org-article:58d327ded9894b2697bd449653a35e312021-12-02T16:52:38ZGenetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations10.1128/mSystems.00493-212379-5077https://doaj.org/article/58d327ded9894b2697bd449653a35e312021-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00493-21https://doaj.org/toc/2379-5077ABSTRACT Hexavalent chromium [Cr(VI)] is a common environmental pollutant. However, little is known about the genetic basis of microbial evolution under Cr(VI) stress and the influence of the prior evolution histories on the subsequent evolution under Cr(VI) stress. In this study, Desulfovibrio vulgaris Hildenborough (DvH), a model sulfate-reducing bacterium, was experimentally evolved for 600 generations. By evolving the replicate populations of three genetically diverse DvH clones, including ancestor (AN, without prior experimental evolution history), non-stress-evolved EC3-10, and salt stress-evolved ES9-11, the contributions of adaptation, chance, and pre-existing genetic divergence to the evolution under Cr(VI) stress were able to be dissected. Significantly decreased lag phases under Cr(VI) stress were observed in most evolved populations, while increased Cr(VI) reduction rates were primarily observed in populations evolved from EC3-10 and ES9-11. The pre-existing genetic divergence in the starting clones showed strong influences on the changes in lag phases, growth rates, and Cr(VI) reduction rates. Additionally, the genomic mutation spectra in populations evolved from different starting clones were significantly different. A total of 14 newly mutated genes obtained mutations in at least two evolved populations, suggesting their importance in Cr(VI) adaptation. An in-frame deletion mutation of one of these genes, the chromate transporter gene DVU0426, demonstrated that it played an important role in Cr(VI) tolerance. Overall, our study identified potential key functional genes for Cr(VI) tolerance and demonstrated the important role of pre-existing genetic divergence in evolution under Cr(VI) stress conditions. IMPORTANCE Chromium is one of the most common heavy metal pollutants of soil and groundwater. The potential of Desulfovibrio vulgaris Hildenborough in heavy metal bioremediation such as Cr(VI) reduction was reported previously; however, experimental evidence of key functional genes involved in Cr(VI) resistance are largely unknown. Given the genetic divergence of microbial populations in nature, knowledge on how this divergence affects the microbial adaptation to a new environment such as Cr(VI) stress is very limited. Taking advantage of our previous study, three groups of genetically diverse D. vulgaris Hildenborough populations with or without prior experimental evolution histories were propagated under Cr(VI) stress for 600 generations. Whole-population genome resequencing of the evolved populations revealed the genomic changes underlying the improved Cr(VI) tolerance. The strong influence of the pre-existing genetic divergence in the starting clones on evolution under Cr(VI) stress conditions was demonstrated at both phenotypic and genetic levels.Weiling ShiQiao MaFeiyan PanYupeng FanMegan L. KempherDaliang NingYuanyuan QuJudy D. WallAifen ZhouJizhong ZhouAmerican Society for Microbiologyarticlechromate stressDesulfovibrio vulgarisexperimental evolutiongenetic backgroundMicrobiologyQR1-502ENmSystems, Vol 6, Iss 3 (2021)
institution DOAJ
collection DOAJ
language EN
topic chromate stress
Desulfovibrio vulgaris
experimental evolution
genetic background
Microbiology
QR1-502
spellingShingle chromate stress
Desulfovibrio vulgaris
experimental evolution
genetic background
Microbiology
QR1-502
Weiling Shi
Qiao Ma
Feiyan Pan
Yupeng Fan
Megan L. Kempher
Daliang Ning
Yuanyuan Qu
Judy D. Wall
Aifen Zhou
Jizhong Zhou
Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations
description ABSTRACT Hexavalent chromium [Cr(VI)] is a common environmental pollutant. However, little is known about the genetic basis of microbial evolution under Cr(VI) stress and the influence of the prior evolution histories on the subsequent evolution under Cr(VI) stress. In this study, Desulfovibrio vulgaris Hildenborough (DvH), a model sulfate-reducing bacterium, was experimentally evolved for 600 generations. By evolving the replicate populations of three genetically diverse DvH clones, including ancestor (AN, without prior experimental evolution history), non-stress-evolved EC3-10, and salt stress-evolved ES9-11, the contributions of adaptation, chance, and pre-existing genetic divergence to the evolution under Cr(VI) stress were able to be dissected. Significantly decreased lag phases under Cr(VI) stress were observed in most evolved populations, while increased Cr(VI) reduction rates were primarily observed in populations evolved from EC3-10 and ES9-11. The pre-existing genetic divergence in the starting clones showed strong influences on the changes in lag phases, growth rates, and Cr(VI) reduction rates. Additionally, the genomic mutation spectra in populations evolved from different starting clones were significantly different. A total of 14 newly mutated genes obtained mutations in at least two evolved populations, suggesting their importance in Cr(VI) adaptation. An in-frame deletion mutation of one of these genes, the chromate transporter gene DVU0426, demonstrated that it played an important role in Cr(VI) tolerance. Overall, our study identified potential key functional genes for Cr(VI) tolerance and demonstrated the important role of pre-existing genetic divergence in evolution under Cr(VI) stress conditions. IMPORTANCE Chromium is one of the most common heavy metal pollutants of soil and groundwater. The potential of Desulfovibrio vulgaris Hildenborough in heavy metal bioremediation such as Cr(VI) reduction was reported previously; however, experimental evidence of key functional genes involved in Cr(VI) resistance are largely unknown. Given the genetic divergence of microbial populations in nature, knowledge on how this divergence affects the microbial adaptation to a new environment such as Cr(VI) stress is very limited. Taking advantage of our previous study, three groups of genetically diverse D. vulgaris Hildenborough populations with or without prior experimental evolution histories were propagated under Cr(VI) stress for 600 generations. Whole-population genome resequencing of the evolved populations revealed the genomic changes underlying the improved Cr(VI) tolerance. The strong influence of the pre-existing genetic divergence in the starting clones on evolution under Cr(VI) stress conditions was demonstrated at both phenotypic and genetic levels.
format article
author Weiling Shi
Qiao Ma
Feiyan Pan
Yupeng Fan
Megan L. Kempher
Daliang Ning
Yuanyuan Qu
Judy D. Wall
Aifen Zhou
Jizhong Zhou
author_facet Weiling Shi
Qiao Ma
Feiyan Pan
Yupeng Fan
Megan L. Kempher
Daliang Ning
Yuanyuan Qu
Judy D. Wall
Aifen Zhou
Jizhong Zhou
author_sort Weiling Shi
title Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations
title_short Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations
title_full Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations
title_fullStr Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations
title_full_unstemmed Genetic Basis of Chromate Adaptation and the Role of the Pre-existing Genetic Divergence during an Experimental Evolution Study with <named-content content-type="genus-species">Desulfovibrio vulgaris</named-content> Populations
title_sort genetic basis of chromate adaptation and the role of the pre-existing genetic divergence during an experimental evolution study with <named-content content-type="genus-species">desulfovibrio vulgaris</named-content> populations
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/58d327ded9894b2697bd449653a35e31
work_keys_str_mv AT weilingshi geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT qiaoma geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT feiyanpan geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT yupengfan geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT meganlkempher geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT daliangning geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT yuanyuanqu geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT judydwall geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT aifenzhou geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
AT jizhongzhou geneticbasisofchromateadaptationandtheroleofthepreexistinggeneticdivergenceduringanexperimentalevolutionstudywithnamedcontentcontenttypegenusspeciesdesulfovibriovulgarisnamedcontentpopulations
_version_ 1718382917965578240