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.

Highlights

  • 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

  • We found operons involved in flagellar biosynthesis such as flg, flh, and fli located in identified genomic islands (GIs) (Table S2C), and the horizontal gene transfer (HGT)-derived chemotaxis operon cheDYBRWAYX was found in all clades of Acidiphilium

  • We suggest that the ancestor of Acidiphilium may have originated in mild or moderate conditions but adapted to extreme environments, such as acid mine drainage (AMD) niches, with the help of HGT and probable positive selection on the genes, similar to what has been found in acidophilic archaeal lineages such as Thermoplasmatales and Sulfolobales, which seemed to have evolved independently from moderately acidophilic ancestors [99]

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Summary

Introduction

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. 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. 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.

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