Integrative Genomics Sheds Light on Evolutionary Forces Shaping the Acidithiobacillia Class Acidophilic Lifestyle

Abstract

Extreme acidophiles thrive in environments rich in protons (pH values <3) and often high levels of dissolved heavy metals. They are distributed across the three domains of the Tree of Life including members of the Proteobacteria. The Acidithiobacillia class is formed by the neutrophilic genus Thermithiobacillus along with the extremely acidophilic genera Fervidacidithiobacillus, Igneacidithiobacillus, Ambacidithiobacillus, and Acidithiobacillus. Phylogenomic reconstruction revealed a division in the Acidithiobacillia class correlating with the different pH optima that suggested that the acidophilic genera evolved from an ancestral neutrophile within the Acidithiobacillia. Genes and mechanisms denominated as “first line of defense” were key to explaining the Acidithiobacillia acidophilic lifestyle including preventing proton influx that allows the cell to maintain a near-neutral cytoplasmic pH and differ from the neutrophilic Acidithiobacillia ancestors that lacked these systems. Additional differences between the neutrophilic and acidophilic Acidithiobacillia included the higher number of gene copies in the acidophilic genera coding for “second line of defense” systems that neutralize and/or expel protons from cell. Gain of genes such as hopanoid biosynthesis involved in membrane stabilization at low pH and the functional redundancy for generating an internal positive membrane potential revealed the transition from neutrophilic properties to a new acidophilic lifestyle by shaping the Acidithiobacillaceae genomic structure. The presence of a pool of accessory genes with functional redundancy provides the opportunity to “hedge bet” in rapidly changing acidic environments. Although a core of mechanisms for acid resistance was inherited vertically from an inferred neutrophilic ancestor, the majority of mechanisms, especially those potentially involved in resistance to extremely low pH, were obtained from other extreme acidophiles by horizontal gene transfer (HGT) events.

Acidithiobacillia class members originating at sites within the Pacific Ring of Fire and other tectonically active locations and description of the novel genus ‘Igneacidithiobacillus’

“…In addition, ‘ Igneacidithiobacillus ’ spp. genomes/MAGs were found to encode genes for the biosynthesis of hopanoids ( hpnABFGHIJKLMN ) ( Supplementary Table S7 ), as all acidophilic members of the Acidithiobacillia class do ( González-Rosales et al, 2022 ), which have been shown to decrease membrane fluidity in bacteria under pH stress ( Sáenz et al, 2015 ).…”

In Silico Characterization of Plant Salt Tolerance Promoting KDP Proteins from Alcaligenes xylosoxydans

“…Present study deals with characterization of the kdpFABC complex in the halotolerant bacterium A. xylosoxydans. Multiple studies identified the presence of kdp ATPaseencoding genes in many halotolerant bacteria, but no one has characterized this complex protein (Gumulya et al, 2018;González-Rosales et al, 2022;Najjari, 2023). Therefore, this is the first-ever study reporting the characterization of proteins constituting the kdp ATPase complex.…”

Understanding a Core Pilin of the Type IVa Pili of Acidithiobacillus thiooxidans, PilV

“…[ 34 ], and González-Rosales et al . [ 35 ]. However, scant attention has been paid to the adaptations of extracellular protein structures, such as T4P, which remain vulnerable to low pH due to their exposure outside the cell.…”