A large-scale genome-based survey of acidophilic Bacteria suggests that genome streamlining is an adaption for life at low pH

Abstract

Genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low nutrient (oligotrophic) and high temperature environments, little work has been carried out on microorganisms from low pH environments and what has been reported is inconclusive. In this study, we performed a large-scale comparative genomics investigation of more than 260 bacterial high-quality genome sequences of acidophiles, together with genomes of their closest phylogenetic relatives that live at circum-neutral pH. A statistically supported correlation is reported between reduction of genome size and decreasing pH that we demonstrate is due to gene loss and reduced gene sizes. This trend is independent from other genome size constraints such as temperature and G+C content. Genome streamlining in the evolution of acidophilic Bacteria is thus supported by our results. Analyses of predicted COG categories and subcellular location predictions indicate that acidophiles have a lower representation of genes encoding extra-cellular proteins, signal transduction mechanisms and proteins with unknown function, but are enriched in inner membrane proteins, chaperones, basic metabolism, and core cellular functions. Contrary to other reports for genome streamlining, there was no significant change in paralog frequencies across pH. However, a detailed analysis of COG categories revealed a higher proportion of genes in acidophiles in the following categories: “Replication and repair”, “Amino acid transport” and “Intracellular trafficking”. This study brings increasing clarity regarding genomic adaptations of acidophiles to life at low pH while putting elements such as the reduction of average gene size under the spotlight of streamlining theory.

Benzo[a]pyrene stress impacts adaptive strategies and ecological functions of earthworm intestinal viromes

“…2A). Metabolic pathways closely related to bacterial survival (nucleotide metabolism and genome replication and repair) [60][61][62] and those associated with bacterial sensing (signal transduction) [63] were significantly enriched in the high-level group (Fig. 2A).…”

Eurypsychrophilic acidophiles: From (meta)genomes to low-temperature biotechnologies

“…In addition, primary and secondary pumps exist that can remove excess cytoplasmic protons (González et al, 2014). Acidophiles also have the capacity to modify and repair DNA as a general response to damage (Parro et al, 2007), and acidophiles may have a streamlined genome in response to their acidic growth pH (Cortez et al, 2022). Finally, the "Fervidacidithiobacillus caldus" (ex-Acidithiobacillus caldus) ferric uptake regulator (Fur) is important in acid resistance and shock by regulating genes involved in, e.g., key genes of certain cellular activities, such as iron transport, biofilm formation, and ISC metabolism (Chen et al, 2020).…”

Genome-guided prediction of acid resistance mechanisms in acidophilic methanotrophs of phylogenetically deep-rooted Verrucomicrobia isolated from geothermal environments

“…All genomes have a contamination index lower than 10% and a completeness index higher than 90% as defined by CheckM. Acidophiles and neutrophiles genome sizes showed differences; the acidophilic clade has an average genome size of 2.37 Mb, in contrast to neutrophiles clades of Opitutales, Chtoniobacterales, and Verrucomicrobiales having an average size of 5.34, 6.3, and 4.28 Mb, respectively (Cortez et al, 2022) (Supplementary Table 1). Genomic indices were calculated to identify the taxonomic rank and species for the genomes under study.…”

“…Reduction of genome size was also observed in the proposed evolutionary trajectory with an average genome size of the neutrophiles of 5.3 Mb, whereas it was 2.37 Mb in the acidophilic clades (Supplementary Table 1). Genome reduction has been proposed to be an adaptive mechanism to reduce energy costs involved in replication and translation in nutrient-scarce environments (Sowell et al, 2009) and under acid stress (Cortez et al, 2022).…”