Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage

ABSTRACT Here, we report three new Acidiphilium genomes, reclassified existing Acidiphilium species, and performed the first comparative genomic analysis on Acidiphilium in an attempt to address the metabolic potential, ecological functions, and evolutionary history of the genus Acidiphilium. In the...

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Autores principales:	Liangzhi Li, Zhenghua Liu, Min Zhang, Delong Meng, Xueduan Liu, Pei Wang, Xiutong Li, Zhen Jiang, Shuiping Zhong, Chengying Jiang, Huaqun Yin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	acid mine drainage evolution horizontal gene transfer comparative genomics Acidiphilium Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c299110b2162411aa51ffb76817d3a28
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spelling	oai:doaj.org-article:c299110b2162411aa51ffb76817d3a282021-12-02T18:15:46ZInsights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage10.1128/mSystems.00867-202379-5077https://doaj.org/article/c299110b2162411aa51ffb76817d3a282020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00867-20https://doaj.org/toc/2379-5077ABSTRACT Here, we report three new Acidiphilium genomes, reclassified existing Acidiphilium species, and performed the first comparative genomic analysis on Acidiphilium in an attempt to address the metabolic potential, ecological functions, and evolutionary history of the genus Acidiphilium. In the genomes of Acidiphilium, we found an abundant repertoire of horizontally transferred genes (HTGs) contributing to environmental adaption and metabolic expansion, including genes conferring photosynthesis (puf, puh), CO2 assimilation (rbc), capacity for methane metabolism (mmo, mdh, frm), nitrogen source utilization (nar, cyn, hmp), sulfur compound utilization (sox, psr, sqr), and multiple metal and osmotic stress resistance capacities (czc, cop, ect). Additionally, the predicted donors of horizontal gene transfer were present in a cooccurrence network of Acidiphilium. Genome-scale positive selection analysis revealed that 15 genes contained adaptive mutations, most of which were multifunctional and played critical roles in the survival of extreme conditions. We proposed that Acidiphilium originated in mild conditions and adapted to extreme environments such as acidic mineral sites after the acquisition of many essential functions. IMPORTANCE Extremophiles, organisms that thrive in extreme environments, are key models for research on biological adaption. They can provide hints for the origin and evolution of life, as well as improve the understanding of biogeochemical cycling of elements. Extremely acidophilic bacteria such as Acidiphilium are widespread in acid mine drainage (AMD) systems, but the metabolic potential, ecological functions, and evolutionary history of this genus are still ambiguous. Here, we sequenced the genomes of three new Acidiphilium strains and performed comparative genomic analysis on this extremely acidophilic bacterial genus. We found in the genomes of Acidiphilium an abundant repertoire of horizontally transferred genes (HTGs) contributing to environmental adaption and metabolic ability expansion, as indicated by phylogenetic reconstruction and gene context comparison. This study has advanced our understanding of microbial evolution and biogeochemical cycling in extreme niches.Liangzhi LiZhenghua LiuMin ZhangDelong MengXueduan LiuPei WangXiutong LiZhen JiangShuiping ZhongChengying JiangHuaqun YinAmerican Society for Microbiologyarticleacid mine drainageevolutionhorizontal gene transfercomparative genomicsAcidiphiliumMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	acid mine drainage evolution horizontal gene transfer comparative genomics Acidiphilium Microbiology QR1-502
spellingShingle	acid mine drainage evolution horizontal gene transfer comparative genomics Acidiphilium Microbiology QR1-502 Liangzhi Li Zhenghua Liu Min Zhang Delong Meng Xueduan Liu Pei Wang Xiutong Li Zhen Jiang Shuiping Zhong Chengying Jiang Huaqun Yin Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage
description	ABSTRACT Here, we report three new Acidiphilium genomes, reclassified existing Acidiphilium species, and performed the first comparative genomic analysis on Acidiphilium in an attempt to address the metabolic potential, ecological functions, and evolutionary history of the genus Acidiphilium. In the genomes of Acidiphilium, we found an abundant repertoire of horizontally transferred genes (HTGs) contributing to environmental adaption and metabolic expansion, including genes conferring photosynthesis (puf, puh), CO2 assimilation (rbc), capacity for methane metabolism (mmo, mdh, frm), nitrogen source utilization (nar, cyn, hmp), sulfur compound utilization (sox, psr, sqr), and multiple metal and osmotic stress resistance capacities (czc, cop, ect). Additionally, the predicted donors of horizontal gene transfer were present in a cooccurrence network of Acidiphilium. Genome-scale positive selection analysis revealed that 15 genes contained adaptive mutations, most of which were multifunctional and played critical roles in the survival of extreme conditions. We proposed that Acidiphilium originated in mild conditions and adapted to extreme environments such as acidic mineral sites after the acquisition of many essential functions. IMPORTANCE Extremophiles, organisms that thrive in extreme environments, are key models for research on biological adaption. They can provide hints for the origin and evolution of life, as well as improve the understanding of biogeochemical cycling of elements. Extremely acidophilic bacteria such as Acidiphilium are widespread in acid mine drainage (AMD) systems, but the metabolic potential, ecological functions, and evolutionary history of this genus are still ambiguous. Here, we sequenced the genomes of three new Acidiphilium strains and performed comparative genomic analysis on this extremely acidophilic bacterial genus. We found in the genomes of Acidiphilium an abundant repertoire of horizontally transferred genes (HTGs) contributing to environmental adaption and metabolic ability expansion, as indicated by phylogenetic reconstruction and gene context comparison. This study has advanced our understanding of microbial evolution and biogeochemical cycling in extreme niches.
format	article
author	Liangzhi Li Zhenghua Liu Min Zhang Delong Meng Xueduan Liu Pei Wang Xiutong Li Zhen Jiang Shuiping Zhong Chengying Jiang Huaqun Yin
author_facet	Liangzhi Li Zhenghua Liu Min Zhang Delong Meng Xueduan Liu Pei Wang Xiutong Li Zhen Jiang Shuiping Zhong Chengying Jiang Huaqun Yin
author_sort	Liangzhi Li
title	Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage
title_short	Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage
title_full	Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage
title_fullStr	Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage
title_full_unstemmed	Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage
title_sort	insights into the metabolism and evolution of the genus <italic toggle="yes">acidiphilium</italic>, a typical acidophile in acid mine drainage
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/c299110b2162411aa51ffb76817d3a28
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Insights into the Metabolism and Evolution of the Genus <italic toggle="yes">Acidiphilium</italic>, a Typical Acidophile in Acid Mine Drainage

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