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Abstract
BackgroundTerrestrial hot spring settings span a broad spectrum of physicochemistries. Physicochemical parameters, such as pH and temperature, are key factors influencing differences in microbial composition across diverse geothermal areas. Nonetheless, analysis of hot spring pools from the Taupo Volcanic Zone (TVZ), New Zealand, revealed that some members of the bacterial genus, Acidithiobacillus, are prevalent across wide ranges of hot spring pHs and temperatures. To determine the genomic attributes of Acidithiobacillus that inhabit such diverse conditions, we assembled the genomes of 19 uncultivated hot spring Acidithiobacillus strains from six geothermal areas and compared these to 37 publicly available Acidithiobacillus genomes from various habitats.ResultsAnalysis of 16S rRNA gene amplicons from 138 samples revealed that Acidithiobacillus comprised on average 11.4 ± 16.8% of hot spring prokaryotic communities, with three Acidithiobacillus amplicon sequence variants (ASVs) (TVZ_G1, TVZ_G2, TVZ_G3) accounting for > 90% of Acidithiobacillus in terms of relative abundance, and occurring in 126 out of 138 samples across wide ranges of temperature (17.5–92.9 °C) and pH (1.0–7.5). We recovered 19 environmental genomes belonging to each of these three ASVs, as well as a fourth related group (TVZ_G4). Based on genome average nucleotide identities, the four groups (TVZ_G1-TVZ_G4) constitute distinct species (ANI < 96.5%) of which three are novel Acidithiobacillus species (TVZ_G2-TVZ_G4) and one belongs to Acidithiobacillus caldus (TVZ_G1). All four TVZ Acidithiobacillus groups were found in hot springs with temperatures above the previously known limit for the genus (up to 40 °C higher), likely due to significantly higher proline and GC contents than other Acidithiobacillus species, which are known to increase thermostability. Results also indicate hot spring-associated Acidithiobacillus have undergone genome streamlining, likely due to thermal adaptation. Moreover, our data suggest that Acidithiobacillus prevalence across varied hot spring pHs is supported by distinct strategies, whereby TVZ_G2-TVZ_G4 regulate pH homeostasis mostly through Na+/H+ antiporters and proton-efflux ATPases, whereas TVZ_G1 mainly relies on amino acid decarboxylases.ConclusionsThis study provides insights into the distribution of Acidithiobacillus species across diverse hot spring physichochemistries and determines genomic features and adaptations that potentially enable Acidithiobacillus species to colonize a broad range of temperatures and pHs in geothermal environments.BoTSrZ5f8ypScVzkmXt8zFVideo
Highlights
Terrestrial hot spring settings span a broad spectrum of physicochemistries
Members of Acidithiobacillus are best known from highly acidic settings, such as ores during bioleaching and acid mine drainage [4, 20], a search of data from almost one thousand Taupo Volcanic Zone (TVZ) hot springs, in New Zealand, showed that Acidithiobacillus are present in springs encompassing a huge range of physicochemistries, from very acidic to alkali pHs (0.6–8.94) and across an extremely wide temperature range (13.9–97.6 °C) [6, 21]
Hot spring characteristics Samples were collected from sulfur-rich hot springs, which are common in the TVZ, and which spanned a broad range of water temperatures (17.5–92.9 °C) to recover mesophilic to hyperthermophilic communities, and pHs (1.0–7.5) to sample acidophilic to neutrophilic communities (Table 1, Fig. S1)
Summary
Terrestrial hot spring settings span a broad spectrum of physicochemistries. Physicochemical parameters, such as pH and temperature, are key factors influencing differences in microbial composition across diverse geothermal areas. Acidithiobacillus (formerly Thiobacillus) is a gramnegative genus of rod-shaped bacteria that mostly comprises chemolithoautotrophic, obligately acidophilic (optimum pH < 4), and mesophilic or mesothermophilic species [1,2,3] They are commonly distributed in acidic and sulfur-rich environments, such as acidic soil and acid mine drainage [4, 5], and recent studies show that they are widely distributed in hot springs [6, 7]. Members of Acidithiobacillus are best known from highly acidic settings, such as ores during bioleaching and acid mine drainage [4, 20], a search of data from almost one thousand Taupo Volcanic Zone (TVZ) hot springs, in New Zealand, showed that Acidithiobacillus are present in springs encompassing a huge range of physicochemistries, from very acidic to alkali pHs (0.6–8.94) and across an extremely wide temperature range (13.9–97.6 °C) [6, 21]
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