Prediction and Inferred Evolution of Acid Tolerance Genes in the Biotechnologically Important Acidihalobacter Genus

Katelyn Boase; Carolina González; Eva Vergara; Gonzalo Neira; David Holmes; Elizabeth Watkin

doi:10.3389/fmicb.2022.848410

Prediction and Inferred Evolution of Acid Tolerance Genes in the Biotechnologically Important Acidihalobacter Genus

Front Microbiol. 2022 Apr 18:13:848410. doi: 10.3389/fmicb.2022.848410. eCollection 2022.

Authors

Katelyn Boase¹, Carolina González², Eva Vergara², Gonzalo Neira², David Holmes^{2

3}, Elizabeth Watkin¹

Affiliations

¹ Curtin Medical School, Curtin University, Perth, WA, Australia.
² Center for Bioinformatics and Genome Biology, Centro Ciencia & Vida, Santiago, Chile.
³ Facultad de Medicina y Ciencias, Universidad San Sebastián, Santiago, Chile.

Abstract

Acidihalobacter is a genus of acidophilic, gram-negative bacteria known for its ability to oxidize pyrite minerals in the presence of elevated chloride ions, a capability rare in other iron-sulfur oxidizing acidophiles. Previous research involving Acidihalobacter spp. has focused on their applicability in saline biomining operations and their genetic arsenal that allows them to cope with chloride, metal and oxidative stress. However, an understanding of the molecular adaptations that enable Acidihalobacter spp. to thrive under both acid and chloride stress is needed to provide a more comprehensive understanding of how this genus can thrive in such extreme biomining conditions. Currently, four genomes of the Acidihalobacter genus have been sequenced: Acidihalobacter prosperus DSM 5130^T, Acidihalobacter yilgarnensis DSM 105917^T, Acidihalobacter aeolianus DSM 14174^T, and Acidihalobacter ferrooxydans DSM 14175^T. Phylogenetic analysis shows that the Acidihalobacter genus roots to the Chromatiales class consisting of mostly halophilic microorganisms. In this study, we aim to advance our knowledge of the genetic repertoire of the Acidihalobacter genus that has enabled it to cope with acidic stress. We provide evidence of gene gain events that are hypothesized to help the Acidihalobacter genus cope with acid stress. Potential acid tolerance mechanisms that were found in the Acidihalobacter genomes include multiple potassium transporters, chloride/proton antiporters, glutamate decarboxylase system, arginine decarboxylase system, urease system, slp genes, squalene synthesis, and hopanoid synthesis. Some of these genes are hypothesized to have entered the Acidihalobacter via vertical decent from an inferred non-acidophilic ancestor, however, horizontal gene transfer (HGT) from other acidophilic lineages is probably responsible for the introduction of many acid resistance genes.

Keywords: acid resistance; chloride/proton antiporters; extreme acidophile; genome evolution; phylogenomics; polyextremophile; potassium transporters; urease.