Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>

ABSTRACT Rapid genetic and phenotypic adaptation of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough to salt stress was observed during experimental evolution. In order to identify key metabolites important for salt tolerance, a clone, ES10-5, which was isolated from population ES...

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Autores principales:	Aifen Zhou, Rebecca Lau, Richard Baran, Jincai Ma, Frederick von Netzer, Weiling Shi, Drew Gorman-Lewis, Megan L. Kempher, Zhili He, Yujia Qin, Zhou Shi, Grant M. Zane, Liyou Wu, Benjamin P. Bowen, Trent R. Northen, Kristina L. Hillesland, David A. Stahl, Judy D. Wall, Adam P. Arkin, Jizhong Zhou
Formato:	article
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Publicado:	American Society for Microbiology 2017
Materias:	Desulfovibrio vulgaris PLFA cell motility energy efficiency genomic mutations organic solutes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0962578a31c94bccb30f1a6a9cc3fe0b
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spelling	oai:doaj.org-article:0962578a31c94bccb30f1a6a9cc3fe0b2021-11-15T15:51:55ZKey Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>10.1128/mBio.01780-172150-7511https://doaj.org/article/0962578a31c94bccb30f1a6a9cc3fe0b2017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01780-17https://doaj.org/toc/2150-7511ABSTRACT Rapid genetic and phenotypic adaptation of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough to salt stress was observed during experimental evolution. In order to identify key metabolites important for salt tolerance, a clone, ES10-5, which was isolated from population ES10 and allowed to experimentally evolve under salt stress for 5,000 generations, was analyzed and compared to clone ES9-11, which was isolated from population ES9 and had evolved under the same conditions for 1,200 generations. These two clones were chosen because they represented the best-adapted clones among six independently evolved populations. ES10-5 acquired new mutations in genes potentially involved in salt tolerance, in addition to the preexisting mutations and different mutations in the same genes as in ES9-11. Most basal abundance changes of metabolites and phospholipid fatty acids (PLFAs) were lower in ES10-5 than ES9-11, but an increase of glutamate and branched PLFA i17:1ω9c under high-salinity conditions was persistent. ES9-11 had decreased cell motility compared to the ancestor; in contrast, ES10-5 showed higher cell motility under both nonstress and high-salinity conditions. Both genotypes displayed better growth energy efficiencies than the ancestor under nonstress or high-salinity conditions. Consistently, ES10-5 did not display most of the basal transcriptional changes observed in ES9-11, but it showed increased expression of genes involved in glutamate biosynthesis, cation efflux, and energy metabolism under high salinity. These results demonstrated the role of glutamate as a key osmolyte and i17:1ω9c as the major PLFA for salt tolerance in D. vulgaris. The mechanistic changes in evolved genotypes suggested that growth energy efficiency might be a key factor for selection. IMPORTANCE High salinity (e.g., elevated NaCl) is a stressor that affects many organisms. Salt tolerance, a complex trait involving multiple cellular pathways, is attractive for experimental evolutionary studies. Desulfovibrio vulgaris Hildenborough is a model sulfate-reducing bacterium (SRB) that is important in biogeochemical cycling of sulfur, carbon, and nitrogen, potentially for bio-corrosion, and for bioremediation of toxic heavy metals and radionuclides. The coexistence of SRB and high salinity in natural habitats and heavy metal-contaminated field sites laid the foundation for the study of salt adaptation of D. vulgaris Hildenborough with experimental evolution. Here, we analyzed a clone that evolved under salt stress for 5,000 generations and compared it to a clone evolved under the same condition for 1,200 generations. The results indicated the key roles of glutamate for osmoprotection and of i17:1ω9c for increasing membrane fluidity during salt adaptation. The findings provide valuable insights about the salt adaptation mechanism changes during long-term experimental evolution.Aifen ZhouRebecca LauRichard BaranJincai MaFrederick von NetzerWeiling ShiDrew Gorman-LewisMegan L. KempherZhili HeYujia QinZhou ShiGrant M. ZaneLiyou WuBenjamin P. BowenTrent R. NorthenKristina L. HilleslandDavid A. StahlJudy D. WallAdam P. ArkinJizhong ZhouAmerican Society for MicrobiologyarticleDesulfovibrio vulgarisPLFAcell motilityenergy efficiencygenomic mutationsorganic solutesMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Desulfovibrio vulgaris PLFA cell motility energy efficiency genomic mutations organic solutes Microbiology QR1-502
spellingShingle	Desulfovibrio vulgaris PLFA cell motility energy efficiency genomic mutations organic solutes Microbiology QR1-502 Aifen Zhou Rebecca Lau Richard Baran Jincai Ma Frederick von Netzer Weiling Shi Drew Gorman-Lewis Megan L. Kempher Zhili He Yujia Qin Zhou Shi Grant M. Zane Liyou Wu Benjamin P. Bowen Trent R. Northen Kristina L. Hillesland David A. Stahl Judy D. Wall Adam P. Arkin Jizhong Zhou Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>
description	ABSTRACT Rapid genetic and phenotypic adaptation of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough to salt stress was observed during experimental evolution. In order to identify key metabolites important for salt tolerance, a clone, ES10-5, which was isolated from population ES10 and allowed to experimentally evolve under salt stress for 5,000 generations, was analyzed and compared to clone ES9-11, which was isolated from population ES9 and had evolved under the same conditions for 1,200 generations. These two clones were chosen because they represented the best-adapted clones among six independently evolved populations. ES10-5 acquired new mutations in genes potentially involved in salt tolerance, in addition to the preexisting mutations and different mutations in the same genes as in ES9-11. Most basal abundance changes of metabolites and phospholipid fatty acids (PLFAs) were lower in ES10-5 than ES9-11, but an increase of glutamate and branched PLFA i17:1ω9c under high-salinity conditions was persistent. ES9-11 had decreased cell motility compared to the ancestor; in contrast, ES10-5 showed higher cell motility under both nonstress and high-salinity conditions. Both genotypes displayed better growth energy efficiencies than the ancestor under nonstress or high-salinity conditions. Consistently, ES10-5 did not display most of the basal transcriptional changes observed in ES9-11, but it showed increased expression of genes involved in glutamate biosynthesis, cation efflux, and energy metabolism under high salinity. These results demonstrated the role of glutamate as a key osmolyte and i17:1ω9c as the major PLFA for salt tolerance in D. vulgaris. The mechanistic changes in evolved genotypes suggested that growth energy efficiency might be a key factor for selection. IMPORTANCE High salinity (e.g., elevated NaCl) is a stressor that affects many organisms. Salt tolerance, a complex trait involving multiple cellular pathways, is attractive for experimental evolutionary studies. Desulfovibrio vulgaris Hildenborough is a model sulfate-reducing bacterium (SRB) that is important in biogeochemical cycling of sulfur, carbon, and nitrogen, potentially for bio-corrosion, and for bioremediation of toxic heavy metals and radionuclides. The coexistence of SRB and high salinity in natural habitats and heavy metal-contaminated field sites laid the foundation for the study of salt adaptation of D. vulgaris Hildenborough with experimental evolution. Here, we analyzed a clone that evolved under salt stress for 5,000 generations and compared it to a clone evolved under the same condition for 1,200 generations. The results indicated the key roles of glutamate for osmoprotection and of i17:1ω9c for increasing membrane fluidity during salt adaptation. The findings provide valuable insights about the salt adaptation mechanism changes during long-term experimental evolution.
format	article
author	Aifen Zhou Rebecca Lau Richard Baran Jincai Ma Frederick von Netzer Weiling Shi Drew Gorman-Lewis Megan L. Kempher Zhili He Yujia Qin Zhou Shi Grant M. Zane Liyou Wu Benjamin P. Bowen Trent R. Northen Kristina L. Hillesland David A. Stahl Judy D. Wall Adam P. Arkin Jizhong Zhou
author_facet	Aifen Zhou Rebecca Lau Richard Baran Jincai Ma Frederick von Netzer Weiling Shi Drew Gorman-Lewis Megan L. Kempher Zhili He Yujia Qin Zhou Shi Grant M. Zane Liyou Wu Benjamin P. Bowen Trent R. Northen Kristina L. Hillesland David A. Stahl Judy D. Wall Adam P. Arkin Jizhong Zhou
author_sort	Aifen Zhou
title	Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>
title_short	Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>
title_full	Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>
title_fullStr	Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>
title_full_unstemmed	Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>
title_sort	key metabolites and mechanistic changes for salt tolerance in an experimentally evolved sulfate-reducing bacterium, <italic toggle="yes">desulfovibrio vulgaris</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/0962578a31c94bccb30f1a6a9cc3fe0b
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Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, <italic toggle="yes">Desulfovibrio vulgaris</italic>

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