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 |
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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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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><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 & 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 & Sons Ltd.</rights><rights>2021 Society for Applied Microbiology and John Wiley & 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 & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><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></search><sort><creationdate>202107</creationdate><title>Mobile genetic elements mediate the mixotrophic evolution of novel Alicyclobacillus species for acid mine drainage adaptation</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a3943-8f07e0c6d39c95ae0edc4f938c3ed1a3de077efbc0c2518e1375dd752fe503f43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acid mine drainage</topic><topic>Alicyclobacillus</topic><topic>Beverages</topic><topic>CRISPR</topic><topic>Gene editing</topic><topic>Genes</topic><topic>Genomes</topic><topic>Genomic islands</topic><topic>Genotypes</topic><topic>Heavy metals</topic><topic>Hot springs</topic><topic>Insertion</topic><topic>Low temperature</topic><topic>Low temperature resistance</topic><topic>Metals</topic><topic>Mine drainage</topic><topic>Oxidation</topic><topic>Oxidation resistance</topic><topic>Phenotypes</topic><topic>Phylogeny</topic><topic>Sediments</topic><topic>Soil</topic><topic>Species</topic><topic>Strains (organisms)</topic><topic>Sulphides</topic><topic>Water pollution</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><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><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Zhenghua</au><au>Liang, Zonglin</au><au>Zhou, Zhicheng</au><au>Li, Liangzhi</au><au>Meng, Delong</au><au>Li, Xiutong</au><au>Tao, Jiemeng</au><au>Jiang, Zhen</au><au>Gu, Yabing</au><au>Huang, Ye</au><au>Liu, Xueduan</au><au>Yang, Zhendong</au><au>Drewniak, Lukasz</au><au>Liu, Tianbo</au><au>Liu, Yongjun</au><au>Liu, Shuangjiang</au><au>Wang, Jianjun</au><au>Jiang, Chengying</au><au>Yin, Huaqun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mobile genetic elements mediate the mixotrophic evolution of novel Alicyclobacillus species for acid mine drainage adaptation</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2021-07</date><risdate>2021</risdate><volume>23</volume><issue>7</issue><spage>3896</spage><epage>3912</epage><pages>3896-3912</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>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.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & 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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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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