Sulfobacillus thermotolerans: new insights into resistance and metabolic capacities of acidophilic chemolithotrophs

Anna E. Panyushkina,Anastasia S. Nikitina,Oksana V. Selezneva,Elena S. Kostryukova,Vladislav V. Babenko,Andrey V. Letarov,Maria A. Letarova,Iraida A. Tsaplina

doi:10.1038/s41598-019-51486-1

Anna E. Panyushkina, Anastasia S. Nikitina + Show 6 more

Open Access

https://doi.org/10.1038/s41598-019-51486-1

Copy DOI

Abstract

The first complete genome of the biotechnologically important species Sulfobacillus thermotolerans has been sequenced. Its 3 317 203-bp chromosome contains an 83 269-bp plasmid-like region, which carries heavy metal resistance determinants and the rusticyanin gene. Plasmid-mediated metal resistance is unusual for acidophilic chemolithotrophs. Moreover, most of their plasmids are cryptic and do not contribute to the phenotype of the host cells. A polyphosphate-based mechanism of metal resistance, which has been previously unknown in the genus Sulfobacillus or other Gram-positive chemolithotrophs, potentially operates in two Sulfobacillus species. The methylcitrate cycle typical for pathogens and identified in the genus Sulfobacillus for the first time can fulfill the energy and/or protective function in S. thermotolerans Kr1 and two other Sulfobacillus species, which have incomplete glyoxylate cycles. It is notable that the TCA cycle, disrupted in all Sulfobacillus isolates under optimal growth conditions, proved to be complete in the cells enduring temperature stress. An efficient antioxidant defense system gives S. thermotolerans another competitive advantage in the microbial communities inhabiting acidic metal-rich environments. The genomic comparisons revealed 80 unique genes in the strain Kr1, including those involved in lactose/galactose catabolism. The results provide new insights into metabolism and resistance mechanisms in the Sulfobacillus genus and other acidophiles.

Highlights

The first complete genome of the biotechnologically important species Sulfobacillus thermotolerans has been sequenced
We focus on the features that have been previously unknown in the genus Sulfobacillus, differentiate S. thermotolerans from other Sulfobacillus organisms or are unusual for acidophilic chemolithotrophs
We identified a putative Pho regulon consisting of phoB, phoR, pstS, pstC, pstA, pstB, and phoU, as well as the ppx and ppk genes, in S. thermotolerans Kr1 and bacteria of the genus Sulfobacillus in general (Fig. 6, Table S7)

Summary

Introduction

The first complete genome of the biotechnologically important species Sulfobacillus thermotolerans has been sequenced. Ferrous iron (Fe2+), elemental sulfur (S0), reduced sulfur compounds (S2−), and hydrogen serve as inorganic electron donors and energy sources in different ACM These characteristics make it possible to use the communities of acidophilic chemolithotrophic bacteria and archaea in biohydrometallurgical (biomining) approaches for the recovery of precious and non-ferrous metals[2,3,4,5,6]. The object of the present research is S. thermotolerans, which is applied in bioleaching/ biooxidation of sulfidic ores and ore concentrates, containing precious (gold and silver) and non-ferrous metals This thermotolerant species is of high industrial importance in the biotechnologies for sulfidic raw material processing at temperatures above 35 °C in the presence of elevated concentrations of toxic components[2,20,28,29,30,31,32]. In contrast to Sulfobacillus species, MIC of Cu2+, Cd2+, Ni2+, and Zn2+ for metal tolerant Cupriavidus metallidurans and Escherichia (E.) coli were 3–13 mM35 and 0.5–4 mM36,37, respectively

Methods

Results

Conclusion