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Mobile genetic elements mediate the mixotrophic evolution of novel Alicyclobacillus species for acid mine drainage adaptation
Authors:Zhenghua Liu  Zonglin Liang  Zhicheng Zhou  Liangzhi Li  Delong Meng  Xiutong Li  Jiemeng Tao  Zhen Jiang  Yabing Gu  Ye Huang  Xueduan Liu  Zhendong Yang  Lukasz Drewniak  Tianbo Liu  Yongjun Liu  Shuangjiang Liu  Jianjun Wang  Chengying Jiang  Huaqun Yin
Institution:1. School of Minerals Processing and Bioengineering, Central South University, Changsha, 410006 China;2. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101 China

University of Chinese Academy of Sciences, Beijing, 100049 China

These authors contributed equally to this work.;3. College of Plant Protection, Hunan Agricultural University, Changsha, 410010 China;4. School of Minerals Processing and Bioengineering, Central South University, Changsha, 410006 China

Key Laboratory of Biometallurgy of Ministry of Education, Central South University, Changsha, 410006 China;5. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101 China

University of Chinese Academy of Sciences, Beijing, 100049 China;6. Department of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, 02-096 Poland;7. Hunan Tobacco Science Institute, Changsha, 410010 China;8. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101 China;9. State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, 210008 China

Abstract: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.
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