Genomic adaptations enabling Acidithiobacillus distribution across wide-ranging hot spring temperatures and pHs

Abstract

Background 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. 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. Results Analysis 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. Conclusions This 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.

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

“…Temperature is negatively correlated with genome size (Pearson’s correlation coefficient, −0.34; p-value, 2.9 * 10 −13 ) (Figure 4A) and G+C is positively correlated with genome size (Pearson’s correlation coefficient, 0.48, p-value 1.9 * 10 −25 ) (Figure 4C). A negative correlation between genome size and temperature has recently been reported for extreme acidophiles of the Acidithiobacillus genus (Sriaporn et. al., 2021).…”

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

“…Analysis revealed that the F. caldus and A. ferrivorans genomes only encoded gad A and they lacked the gad C antiporter ( Mangold et al, 2011 ). However, it is proposed that the decarboxylated GABA product from glutamate decarboxylation might be retained in the cell where it can be incorporated into the TCA cycle ( Karatzas et al, 2010 ; Feehily and Karatzas, 2013 ; Sriaporn et al, 2021 ). Even though a complete glutamate decarboxylase exporting system was not identified, previous studies have shown that amino acid decarboxylation is highly expressed in F. caldus under acid stress conditions ( Mangold et al, 2013 ; Sriaporn et al, 2021 ).…”

“…However, it is proposed that the decarboxylated GABA product from glutamate decarboxylation might be retained in the cell where it can be incorporated into the TCA cycle ( Karatzas et al, 2010 ; Feehily and Karatzas, 2013 ; Sriaporn et al, 2021 ). Even though a complete glutamate decarboxylase exporting system was not identified, previous studies have shown that amino acid decarboxylation is highly expressed in F. caldus under acid stress conditions ( Mangold et al, 2013 ; Sriaporn et al, 2021 ). The adi A gene contained the domain spe A that also participates in putrescine synthesis and explains why this gene is associated with both pathways ( adi A- spe A; Figure 7 ).…”

“…Low pH mitigation mechanisms have been investigated in acidophiles ( Baker-Austin and Dopson, 2007 ; Li et al, 2011 ; Ullrich et al, 2016a ; Colman et al, 2018 ; Vergara et al, 2020 ; Chen et al, 2021 ; Mayer et al, 2021 ; Sriaporn et al, 2021 ). These studies show that horizontal gene transfer (HGT), gene mutation, and gene loss trajectories in evolution allow adaptation and survival of prokaryotes in extreme conditions ( Foster, 2004 ; Ullrich et al, 2016a ; Zhang et al, 2017 ; Vergara et al, 2020 ).…”

“…Three populations of uncultivated hot spring Acidithiobacillus strains and ten publicly available genomes were analyzed for the presence or absence of predicted genes for acid resistance, identifying a similar number of gene copies encoding for K + transporters, deiminases/deaminase group and adenosine deaminase shared between genomes, and a difference in the number of amino acid decarboxylases, Na + /H + antiporters, and plasma membrane proton-efflux P-type ATPases ( Sriaporn et al, 2021 ). In addition, the mechanisms of resistance to low temperature and pH from an extreme microbial community where A. ferrivorans was the dominant member revealed an adaptation to low temperature by the presence trehalose synthase pathways, oxidative stress pathways, cold shock proteins, and genes encoding for biofilm formation ( González et al, 2014 ; Liljeqvist et al, 2015 ).…”