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Desiccation induces varied responses within a soil bacterial genus
Desiccation impacts a suite of physiological processes in microbes by elevating levels of damaging reactive oxygen species and inducing DNA strand breaks. In response to desiccation‐induced stress, microbes have evolved specialized mechanisms to help them survive. Here, we performed a 128‐day lab de...
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Published in: | Environmental microbiology 2023-12, Vol.25 (12), p.3075-3086 |
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description | Desiccation impacts a suite of physiological processes in microbes by elevating levels of damaging reactive oxygen species and inducing DNA strand breaks. In response to desiccation‐induced stress, microbes have evolved specialized mechanisms to help them survive. Here, we performed a 128‐day lab desiccation experiment on nine strains from three clades of an abundant soil bacterium, Curtobacterium. We sequenced RNA from each strain at three time points to investigate their response. Curtobacterium was highly resistant to desiccation, outlasting both Escherichia coli and a famously DNA damage‐resistant bacterium, Deinococcus radiodurans. However, within the genus, there were also 10‐fold differences in survival rates among strains. Transcriptomic profiling revealed responses shared within the genus including up‐regulation of genes involved in DNA damage repair, osmolyte production, and efflux pumps, but also up‐regulation of pathways and genes unique to the three clades. For example, trehalose synthesis gene otsB, the chaperone groEL, and the oxygen scavenger katA were all found in either one or two clades but not the third. Here, we provide evidence of considerable variation in closely related strains, and further elucidation of the phylogenetic conservation of desiccation tolerance remains an important goal for microbial ecologists.
Moisture stress in soils is widespread, but much of what is known about how bacteria survive desiccation is from food‐borne human pathogens. Given that drought is becoming increasingly common in soil environments, there is a growing importance of understanding how free‐living bacteria survive desiccation. Here, we investigated the desiccation response in an abundant soil bacterium, Curtobacterium. We found that while many genetic mechanisms seemed to be conserved with other bacteria, this complex trait also varies within the genus. Such investigations will be critical in furthering our understanding of the evolutionary context of this important microbial trait. |
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Moisture stress in soils is widespread, but much of what is known about how bacteria survive desiccation is from food‐borne human pathogens. Given that drought is becoming increasingly common in soil environments, there is a growing importance of understanding how free‐living bacteria survive desiccation. Here, we investigated the desiccation response in an abundant soil bacterium, Curtobacterium. We found that while many genetic mechanisms seemed to be conserved with other bacteria, this complex trait also varies within the genus. Such investigations will be critical in furthering our understanding of the evolutionary context of this important microbial trait.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.16494</identifier><identifier>PMID: 37664956</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Bacteria ; Curtobacterium ; Damage ; Deoxyribonucleic acid ; Desiccation ; DNA ; DNA Damage ; DNA Repair ; E coli ; Ecologists ; Efflux ; Gene regulation ; Genes ; Microbiological strains ; Microorganisms ; Oxygen ; Phylogenetics ; Phylogeny ; Reactive oxygen species ; Soil bacteria ; Soil microorganisms ; Soils ; Strains (organisms) ; Survival ; Transcriptomics ; Trehalose</subject><ispartof>Environmental microbiology, 2023-12, Vol.25 (12), p.3075-3086</ispartof><rights>2023 The Authors. published by Applied Microbiology International and John Wiley & Sons Ltd.</rights><rights>2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4394-f966b11939d99262c79d2395e8e137754a2b958b262d1552e5d9b9c08264c83</citedby><cites>FETCH-LOGICAL-c4394-f966b11939d99262c79d2395e8e137754a2b958b262d1552e5d9b9c08264c83</cites><orcidid>0000-0002-2415-1247 ; 0000-0001-6331-1840 ; 0000000224151247 ; 0000000163311840</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37664956$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1998012$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Scales, N. C.</creatorcontrib><creatorcontrib>Huynh, K. T.</creatorcontrib><creatorcontrib>Weihe, C.</creatorcontrib><creatorcontrib>Martiny, J. B. H.</creatorcontrib><title>Desiccation induces varied responses within a soil bacterial genus</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Desiccation impacts a suite of physiological processes in microbes by elevating levels of damaging reactive oxygen species and inducing DNA strand breaks. In response to desiccation‐induced stress, microbes have evolved specialized mechanisms to help them survive. Here, we performed a 128‐day lab desiccation experiment on nine strains from three clades of an abundant soil bacterium, Curtobacterium. We sequenced RNA from each strain at three time points to investigate their response. Curtobacterium was highly resistant to desiccation, outlasting both Escherichia coli and a famously DNA damage‐resistant bacterium, Deinococcus radiodurans. However, within the genus, there were also 10‐fold differences in survival rates among strains. Transcriptomic profiling revealed responses shared within the genus including up‐regulation of genes involved in DNA damage repair, osmolyte production, and efflux pumps, but also up‐regulation of pathways and genes unique to the three clades. For example, trehalose synthesis gene otsB, the chaperone groEL, and the oxygen scavenger katA were all found in either one or two clades but not the third. Here, we provide evidence of considerable variation in closely related strains, and further elucidation of the phylogenetic conservation of desiccation tolerance remains an important goal for microbial ecologists.
Moisture stress in soils is widespread, but much of what is known about how bacteria survive desiccation is from food‐borne human pathogens. Given that drought is becoming increasingly common in soil environments, there is a growing importance of understanding how free‐living bacteria survive desiccation. Here, we investigated the desiccation response in an abundant soil bacterium, Curtobacterium. We found that while many genetic mechanisms seemed to be conserved with other bacteria, this complex trait also varies within the genus. Such investigations will be critical in furthering our understanding of the evolutionary context of this important microbial trait.</description><subject>Bacteria</subject><subject>Curtobacterium</subject><subject>Damage</subject><subject>Deoxyribonucleic acid</subject><subject>Desiccation</subject><subject>DNA</subject><subject>DNA Damage</subject><subject>DNA Repair</subject><subject>E coli</subject><subject>Ecologists</subject><subject>Efflux</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Microbiological strains</subject><subject>Microorganisms</subject><subject>Oxygen</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Reactive oxygen species</subject><subject>Soil bacteria</subject><subject>Soil microorganisms</subject><subject>Soils</subject><subject>Strains (organisms)</subject><subject>Survival</subject><subject>Transcriptomics</subject><subject>Trehalose</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqFkbtPwzAQxi0E4j2zoQgWllI_Eic38gYJxAC75ThXapTaxU5A_Pe4TenAwsnSnc-_-yR_R8gRo-csxZjlko848HSVOeQbZHfd2VzXjO-QvRjfKWWlKOk22RGlTHghd8nlNUZrjO6sd5l1TW8wZp86WGyygHHuXUyNL9tNrct0Fr1ts1qbDoPVbfaGro8HZGui24iHq7xPXm5vXq_uR4_Pdw9XF48jkwvIRxOQsmYMBDQAXHJTQsMFFFghE2VZ5JrXUFR1empYUXAsGqjB0IrL3FRin5wMqj52VkVjOzRT451D0ykGUFHGE3Q2QPPgP3qMnZrZaLBttUPfR8UrSSUDuURP_6Dvvg8ufUBxoEKkI0WixgNlgo8x4ETNg53p8K0YVYsNqIXHauG3Wm4gTRyvdPt6hs2a_7U8AcUAfNkWv__TUzdPD4PwDxFwjLw</recordid><startdate>202312</startdate><enddate>202312</enddate><creator>Scales, N. 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Moisture stress in soils is widespread, but much of what is known about how bacteria survive desiccation is from food‐borne human pathogens. Given that drought is becoming increasingly common in soil environments, there is a growing importance of understanding how free‐living bacteria survive desiccation. Here, we investigated the desiccation response in an abundant soil bacterium, Curtobacterium. We found that while many genetic mechanisms seemed to be conserved with other bacteria, this complex trait also varies within the genus. Such investigations will be critical in furthering our understanding of the evolutionary context of this important microbial trait.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>37664956</pmid><doi>10.1111/1462-2920.16494</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-2415-1247</orcidid><orcidid>https://orcid.org/0000-0001-6331-1840</orcidid><orcidid>https://orcid.org/0000000224151247</orcidid><orcidid>https://orcid.org/0000000163311840</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Curtobacterium Damage Deoxyribonucleic acid Desiccation DNA DNA Damage DNA Repair E coli Ecologists Efflux Gene regulation Genes Microbiological strains Microorganisms Oxygen Phylogenetics Phylogeny Reactive oxygen species Soil bacteria Soil microorganisms Soils Strains (organisms) Survival Transcriptomics Trehalose |
title | Desiccation induces varied responses within a soil bacterial genus |
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