Metabolic diversity and adaptive mechanisms of iron‐ and/or sulfur‐oxidizing autotrophic acidophiles in extremely acidic environments

Abstract

Many studies have investigated the mechanisms underlying the survival and growth of certain organisms in extremely acidic environments known to be harmful to most prokaryotes and eukaryotes. Acidithiobacillus and Leptospirillum spp. are dominant bioleaching bacteria widely used in bioleaching systems, which are characterized by extremely acidic environments. To survive and grow in such settings, these acidophiles utilize shared molecular mechanisms that allow life in extreme conditions. In this review, we have summarized the results of published genomic analyses, which underscore the ability of iron- and/or sulfur-oxidizing autotrophic acidophiles belonging to the genera Acidithiobacillus and Leptospirillum to adapt to acidic environmental conditions. Several lines of evidence point at the metabolic diversity and multiplicity of pathways involved in the survival of these organisms. The ability to thrive in adverse environments requires versatile activation of structural and functional adaptive responses, including bacterial adhesion, motility, and resistance to heavy metals. We have highlighted recent developments centered on the key survival mechanisms employed by dominant extremophiles, and have laid the foundation for future studies focused on the ability of acidophiles to thrive in extremely acidic environments.

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

“…Similar to the published Sulfobacillus genomes (30, 31), a full suite of genes involved in the Calvin-Benson-Bassham cycle were predicted in all strains ( Fig. 3 and Table S4), e.g., form I ribulose 1,5-bisphosphate carboxylase (RuBisCO), composed of eight large and eight small subunits (27). In chemolithoautotrophic acidophiles, such as Acidithiobacillus and Ferrovum spp., a gene cluster potentially encoding several copies FIG 3 Schematic representation of the predicted metabolic potentials and adaptive strategies for environmental stresses within Sulfobacillus strains.…”

“…CBB, Calvin-Benson-Bassham cycle; CoA, coenzyme A; cyt, cytochrome; Hyd Grp., hydrogenase group. of carboxysome shell proteins, carboxysome-associated carbonic anhydrase, and RuBisCO were identified (9,27,43,44). These microorganisms utilize carboxysomeassociated carbonic anhydrase to elevate the concentration of carbon dioxide near the RuBisCO via conversion of accumulated cytoplasmic bicarbonate into CO 2 (52), thereby enabling efficient utilization of the limited available carbon in the environment.…”

“…Several Sulfobacillus isolates have been recognized as iron oxidizers (33,(37)(38)(39). In other acidophiles, such as Acidithiobacillus ferrooxidans (27), electrons derived from iron oxidation are ultimately transferred to either terminal electron acceptor NADH dehydrogenase ("uphill") or to molecular oxygen ("downhill"). Similarly, S. thermosulfidooxidans and Sulfobacillus sp.…”

“…A strategy to engineer the Streptomyces avermitilis genome has been performed, in which nonessential segments are deleted (79,80) to improve the expression of heterologous pathways (81). Because acidic habitats have nutrient-deficient substrates (27), genome reduction appears to confer adaptive fitness advantages that drive the abandonment of expensive genes, thereby enabling the effective acquisition of limited nutrients. For long-term evolution, the streamlining process has allowed bacteria to maintain essential genes, as well as facilitate in the loss of dispensable ones, thereby resulting in a simpler but still fully functional genome.…”

“…However, microorganisms have been widely found in habitats that are characterized by harsh attributes, such as high temperature (25), high salinity (26), low pH (27,28), or under strictly anaerobic conditions (29). To adapt to short-term or longstanding environmental stresses, microbes may have undergone frequent gene turnover.…”