Mobile genetic elements mediate the mixotrophic evolution of novel Alicyclobacillus species for acid mine drainage adaptation

Summary Alicyclobacillus species inhabit diverse environments and have adapted to broad ranges of pH and temperature. However, their adaptive evolutions remain elusive, especially regarding the role of mobile genetic elements (MGEs). Here, we characterized the distributions and functions of MGEs in...

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Veröffentlicht in:Environmental microbiology 2021-07, Vol.23 (7), p.3896-3912
Hauptverfasser: Liu, Zhenghua, Liang, Zonglin, Zhou, Zhicheng, Li, Liangzhi, Meng, Delong, Li, Xiutong, Tao, Jiemeng, Jiang, Zhen, Gu, Yabing, Huang, Ye, Liu, Xueduan, Yang, Zhendong, Drewniak, Lukasz, Liu, Tianbo, Liu, Yongjun, Liu, Shuangjiang, Wang, Jianjun, Jiang, Chengying, Yin, Huaqun
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container_end_page 3912
container_issue 7
container_start_page 3896
container_title Environmental microbiology
container_volume 23
creator Liu, Zhenghua
Liang, Zonglin
Zhou, Zhicheng
Li, Liangzhi
Meng, Delong
Li, Xiutong
Tao, Jiemeng
Jiang, Zhen
Gu, Yabing
Huang, Ye
Liu, Xueduan
Yang, Zhendong
Drewniak, Lukasz
Liu, Tianbo
Liu, Yongjun
Liu, Shuangjiang
Wang, Jianjun
Jiang, Chengying
Yin, Huaqun
description Summary Alicyclobacillus species inhabit diverse environments and have adapted to broad ranges of pH and temperature. However, their adaptive evolutions remain elusive, especially regarding the role of mobile genetic elements (MGEs). Here, we characterized the distributions and functions of MGEs in Alicyclobacillus species across five environments, including acid mine drainage (AMD), beverages, hot springs, sediments, and soils. Nine Alicyclobacillus strains were isolated from AMD and possessed larger genome sizes and more genes than those from other environments. Four AMD strains evolved to be mixotrophic and fell into distinctive clusters in phylogenetic tree. Four types of MGEs including genomic island (GI), insertion sequence (IS), prophage, and integrative and conjugative element (ICE) were widely distributed in Alicyclobacillus species. Further, AMD strains did not possess CRISPR‐Cas systems, but had more GI, IS, and ICE, as well as more MGE‐associated genes involved in the oxidation of iron and sulfide and the resistance of heavy metal and low temperature. These findings highlight the differences in phenotypes and genotypes between strains isolated from AMD and other environments and the important role of MGEs in rapid environment niche expansions.
doi_str_mv 10.1111/1462-2920.15543
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However, their adaptive evolutions remain elusive, especially regarding the role of mobile genetic elements (MGEs). Here, we characterized the distributions and functions of MGEs in Alicyclobacillus species across five environments, including acid mine drainage (AMD), beverages, hot springs, sediments, and soils. Nine Alicyclobacillus strains were isolated from AMD and possessed larger genome sizes and more genes than those from other environments. Four AMD strains evolved to be mixotrophic and fell into distinctive clusters in phylogenetic tree. Four types of MGEs including genomic island (GI), insertion sequence (IS), prophage, and integrative and conjugative element (ICE) were widely distributed in Alicyclobacillus species. Further, AMD strains did not possess CRISPR‐Cas systems, but had more GI, IS, and ICE, as well as more MGE‐associated genes involved in the oxidation of iron and sulfide and the resistance of heavy metal and low temperature. These findings highlight the differences in phenotypes and genotypes between strains isolated from AMD and other environments and the important role of MGEs in rapid environment niche expansions.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.15543</identifier><identifier>PMID: 33913568</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley &amp; Sons, Inc</publisher><subject>Acid mine drainage ; Alicyclobacillus ; Beverages ; CRISPR ; Gene editing ; Genes ; Genomes ; Genomic islands ; Genotypes ; Heavy metals ; Hot springs ; Insertion ; Low temperature ; Low temperature resistance ; Metals ; Mine drainage ; Oxidation ; Oxidation resistance ; Phenotypes ; Phylogeny ; Sediments ; Soil ; Species ; Strains (organisms) ; Sulphides ; Water pollution</subject><ispartof>Environmental microbiology, 2021-07, Vol.23 (7), p.3896-3912</ispartof><rights>2021 Society for Applied Microbiology and John Wiley &amp; Sons Ltd.</rights><rights>2021 Society for Applied Microbiology and John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a3943-8f07e0c6d39c95ae0edc4f938c3ed1a3de077efbc0c2518e1375dd752fe503f43</citedby><cites>FETCH-LOGICAL-a3943-8f07e0c6d39c95ae0edc4f938c3ed1a3de077efbc0c2518e1375dd752fe503f43</cites><orcidid>0000-0002-9857-2941 ; 0000-0002-7585-310X ; 0000-0001-7039-7136 ; 0000-0002-1215-001X ; 0000-0002-3236-0508</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.15543$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.15543$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,27922,27923,45572,45573</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33913568$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Zhenghua</creatorcontrib><creatorcontrib>Liang, Zonglin</creatorcontrib><creatorcontrib>Zhou, Zhicheng</creatorcontrib><creatorcontrib>Li, Liangzhi</creatorcontrib><creatorcontrib>Meng, Delong</creatorcontrib><creatorcontrib>Li, Xiutong</creatorcontrib><creatorcontrib>Tao, Jiemeng</creatorcontrib><creatorcontrib>Jiang, Zhen</creatorcontrib><creatorcontrib>Gu, Yabing</creatorcontrib><creatorcontrib>Huang, Ye</creatorcontrib><creatorcontrib>Liu, Xueduan</creatorcontrib><creatorcontrib>Yang, Zhendong</creatorcontrib><creatorcontrib>Drewniak, Lukasz</creatorcontrib><creatorcontrib>Liu, Tianbo</creatorcontrib><creatorcontrib>Liu, Yongjun</creatorcontrib><creatorcontrib>Liu, Shuangjiang</creatorcontrib><creatorcontrib>Wang, Jianjun</creatorcontrib><creatorcontrib>Jiang, Chengying</creatorcontrib><creatorcontrib>Yin, Huaqun</creatorcontrib><title>Mobile genetic elements mediate the mixotrophic evolution of novel Alicyclobacillus species for acid mine drainage adaptation</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary Alicyclobacillus species inhabit diverse environments and have adapted to broad ranges of pH and temperature. However, their adaptive evolutions remain elusive, especially regarding the role of mobile genetic elements (MGEs). Here, we characterized the distributions and functions of MGEs in Alicyclobacillus species across five environments, including acid mine drainage (AMD), beverages, hot springs, sediments, and soils. Nine Alicyclobacillus strains were isolated from AMD and possessed larger genome sizes and more genes than those from other environments. Four AMD strains evolved to be mixotrophic and fell into distinctive clusters in phylogenetic tree. Four types of MGEs including genomic island (GI), insertion sequence (IS), prophage, and integrative and conjugative element (ICE) were widely distributed in Alicyclobacillus species. Further, AMD strains did not possess CRISPR‐Cas systems, but had more GI, IS, and ICE, as well as more MGE‐associated genes involved in the oxidation of iron and sulfide and the resistance of heavy metal and low temperature. These findings highlight the differences in phenotypes and genotypes between strains isolated from AMD and other environments and the important role of MGEs in rapid environment niche expansions.</description><subject>Acid mine drainage</subject><subject>Alicyclobacillus</subject><subject>Beverages</subject><subject>CRISPR</subject><subject>Gene editing</subject><subject>Genes</subject><subject>Genomes</subject><subject>Genomic islands</subject><subject>Genotypes</subject><subject>Heavy metals</subject><subject>Hot springs</subject><subject>Insertion</subject><subject>Low temperature</subject><subject>Low temperature resistance</subject><subject>Metals</subject><subject>Mine drainage</subject><subject>Oxidation</subject><subject>Oxidation resistance</subject><subject>Phenotypes</subject><subject>Phylogeny</subject><subject>Sediments</subject><subject>Soil</subject><subject>Species</subject><subject>Strains (organisms)</subject><subject>Sulphides</subject><subject>Water pollution</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkT1PBCEQhonR-F3bGRIbm1NYlmO3NMavRGOjNeFgODHsssKueoX_XdY7r7CRBpg882QyL0JHlJzRfM5pOS0mRV3kL-cl20C768rm-k2LHbSX0ishVDBBttEOYzVlfFrtoq-HMHMe8Bxa6J3G4KGBtk-4AeNUD7h_Ady4z9DH0L2MwHvwQ-9Ci4PFbXgHjy-80wvtw0xp5_2QcOpAO0jYhohzzWRBC9hE5Vo1B6yM6no1Og7QllU-weHq3kfP11dPl7eT-8ebu8uL-4lidckmlSUCiJ4aVuuaKyBgdGlrVmkGhipmgAgBdqaJLjitgDLBjRG8sMAJsyXbR6dLbxfD2wCpl41LGrxXLYQhydxVV6RiVZXRkz_oaxhim6fLFJ_SUoiCZOp8SekYUopgZRddo-JCUiLHZOS4eznmIH-SyR3HK-8wy7td879RZIAvgY-cx-I_n7x6uFuKvwHYmpoA</recordid><startdate>202107</startdate><enddate>202107</enddate><creator>Liu, Zhenghua</creator><creator>Liang, Zonglin</creator><creator>Zhou, Zhicheng</creator><creator>Li, Liangzhi</creator><creator>Meng, Delong</creator><creator>Li, Xiutong</creator><creator>Tao, Jiemeng</creator><creator>Jiang, Zhen</creator><creator>Gu, Yabing</creator><creator>Huang, Ye</creator><creator>Liu, Xueduan</creator><creator>Yang, Zhendong</creator><creator>Drewniak, Lukasz</creator><creator>Liu, Tianbo</creator><creator>Liu, Yongjun</creator><creator>Liu, Shuangjiang</creator><creator>Wang, Jianjun</creator><creator>Jiang, Chengying</creator><creator>Yin, Huaqun</creator><general>John Wiley &amp; 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However, their adaptive evolutions remain elusive, especially regarding the role of mobile genetic elements (MGEs). Here, we characterized the distributions and functions of MGEs in Alicyclobacillus species across five environments, including acid mine drainage (AMD), beverages, hot springs, sediments, and soils. Nine Alicyclobacillus strains were isolated from AMD and possessed larger genome sizes and more genes than those from other environments. Four AMD strains evolved to be mixotrophic and fell into distinctive clusters in phylogenetic tree. Four types of MGEs including genomic island (GI), insertion sequence (IS), prophage, and integrative and conjugative element (ICE) were widely distributed in Alicyclobacillus species. Further, AMD strains did not possess CRISPR‐Cas systems, but had more GI, IS, and ICE, as well as more MGE‐associated genes involved in the oxidation of iron and sulfide and the resistance of heavy metal and low temperature. These findings highlight the differences in phenotypes and genotypes between strains isolated from AMD and other environments and the important role of MGEs in rapid environment niche expansions.</abstract><cop>Hoboken, USA</cop><pub>John Wiley &amp; Sons, Inc</pub><pmid>33913568</pmid><doi>10.1111/1462-2920.15543</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-9857-2941</orcidid><orcidid>https://orcid.org/0000-0002-7585-310X</orcidid><orcidid>https://orcid.org/0000-0001-7039-7136</orcidid><orcidid>https://orcid.org/0000-0002-1215-001X</orcidid><orcidid>https://orcid.org/0000-0002-3236-0508</orcidid></addata></record>
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source Wiley Online Library All Journals
subjects Acid mine drainage
Alicyclobacillus
Beverages
CRISPR
Gene editing
Genes
Genomes
Genomic islands
Genotypes
Heavy metals
Hot springs
Insertion
Low temperature
Low temperature resistance
Metals
Mine drainage
Oxidation
Oxidation resistance
Phenotypes
Phylogeny
Sediments
Soil
Species
Strains (organisms)
Sulphides
Water pollution
title Mobile genetic elements mediate the mixotrophic evolution of novel Alicyclobacillus species for acid mine drainage adaptation
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