Abstract

Members of the genus Metallosphaera are widely found in sulfur-rich and metal-laden environments, but their physiological and ecological roles remain poorly understood. Here, we sequenced Metallosphaera tengchongensis Ric-A, a strain isolated from the Tengchong hot spring in Yunnan Province, China, and performed a comparative genome analysis with other Metallosphaera genomes. The genome of M. tengchongensis had an average nucleotide identity (ANI) of approximately 70% to that of Metallosphaera cuprina. Genes sqr, tth, sir, tqo, hdr, tst, soe, and sdo associated with sulfur oxidation, and gene clusters fox and cbs involved in iron oxidation existed in all Metallosphaera genomes. However, the adenosine-5′-phosphosulfate (APS) pathway was only detected in Metallosphaera sedula and Metallosphaera yellowstonensis, and several subunits of fox cluster were lost in M. cuprina. The complete 3-hydroxypropionate/4-hydroxybutyrate cycle and dicarboxylate/4-hydroxybutyrate cycle involved in carbon fixation were found in all Metallosphaera genomes. A large number of gene family gain events occurred in M. yellowstonensis and M. sedula, whereas gene family loss events occurred frequently in M. cuprina. Pervasive strong purifying selection was found acting on the gene families of Metallosphaera, of which transcription-related genes underwent the strongest purifying selection. In contrast, genes related to prophages, transposons, and defense mechanisms were under weaker purifying pressure. Taken together, this study expands knowledge of the genomic traits of Metallosphaera species and sheds light on their evolution.

Highlights

  • Acidophilic archaea of the genus Metallosphaera belong to the order Sulfolobales within the Crenarchaeota

  • The adenosine-5 -phosphosulfate (APS) pathway was only detected in M. sedula and M. yellowstonensis, and certain subunits of the fox cluster were lost in M. cuprina

  • The genes for assimilatory nitrate reduction were present in all genomes of 19 strains; a complete dissimilatory nitrate reductase gene cluster was only found in M. yellowstonensis, which demonstrated that Metallosphaera species and strains have different abilities to use inorganic nitrogen

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Summary

Introduction

Acidophilic archaea of the genus Metallosphaera belong to the order Sulfolobales within the Crenarchaeota. Members of the genus Metallosphaera grow aerobically at low pH values (60◦C). They are found in sulfur-rich and metal-laden environments including solfataric areas (Metallosphaera sedula DSM 5348 and strains from laboratory evolution) (Huber et al, 1989; Ai et al, 2016, 2017), hot springs Metallosphaera species are of great potential in the extraction of base and precious metals from ores exploiting their ability to oxidize reduced inorganic sulfur compounds (RISCs) and ferrous ion, a process mediated by a set of terminal oxidases that are attached to their cell membranes (Auernik and Kelly, 2008, 2010; Orell et al, 2010). Previous studies showed that application of thermophilic archaea in chalcopyrite bioleaching could achieve faster dissolution rates and higher copper leaching yields in comparison to widely used mesophilic bioleaching bacteria because the formation of the surface passivation and diffusion layer of chalcopyrite was significantly reduced at high temperature (Rawlings, 2005; Urbieta et al, 2015; Castro and Donati, 2016)

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