Abstract

Acidithiobacillus caldus is an extremely acidophilic sulfur-oxidizer with specialized characteristics, such as tolerance to low pH and heavy metal resistance. To gain novel insights into its genetic complexity, we chosen six A. caldus strains for comparative survey. All strains analyzed in this study differ in geographic origins as well as in ecological preferences. Based on phylogenomic analysis, we clustered the six A. caldus strains isolated from various ecological niches into two groups: group 1 strains with smaller genomes and group 2 strains with larger genomes. We found no obvious intraspecific divergence with respect to predicted genes that are related to central metabolism and stress management strategies between these two groups. Although numerous highly homogeneous genes were observed, high genetic diversity was also detected. Preliminary inspection provided a first glimpse of the potential correlation between intraspecific diversity at the genome level and environmental variation, especially geochemical conditions. Evolutionary genetic analyses further showed evidence that the difference in environmental conditions might be a crucial factor to drive the divergent evolution of A. caldus species. We identified a diverse pool of mobile genetic elements including insertion sequences and genomic islands, which suggests a high frequency of genetic exchange in these harsh habitats. Comprehensive analysis revealed that gene gains and losses were both dominant evolutionary forces that directed the genomic diversification of A. caldus species. For instance, horizontal gene transfer and gene duplication events in group 2 strains might contribute to an increase in microbial DNA content and novel functions. Moreover, genomes undergo extensive changes in group 1 strains such as removal of potential non-functional DNA, which results in the formation of compact and streamlined genomes. Taken together, the findings presented herein show highly frequent gene turnover of A. caldus species that inhabit extremely acidic environments, and shed new light on the contribution of gene turnover to the evolutionary adaptation of acidophiles.

Highlights

  • Acidithiobacillus caldus, a moderately thermophilic, obligately chemolithoautotrophic, and extremely acidophilic sulfur-oxidizing bacterium (Hallberg and Lindström, 1994, 1996), is of interest for its potential role in industrial bioleaching (Rawlings, 1998; Dopson and Lindström, 1999)

  • Genome-size variations in bacteria correspond to variations in gene number as bacterial genomes are tightly packed, and most sequences are functional protein-coding regions (Mira et al, 2001)

  • It might be reasonable considering that A. caldus species was known as the only known mesothermophile within the Acidithiobacillales (Acuña et al, 2013), and GC content of prokaryotic genomes was positively correlated with optimal growth temperature (Musto et al, 2004, 2006)

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Summary

Introduction

Acidithiobacillus caldus (formerly Thiobacillus caldus), a moderately thermophilic, obligately chemolithoautotrophic, and extremely acidophilic sulfur-oxidizing bacterium (Hallberg and Lindström, 1994, 1996), is of interest for its potential role in industrial bioleaching (Rawlings, 1998; Dopson and Lindström, 1999). A. caldus exploits elemental sulfur and a wide range of reduced inorganic sulfur compounds at moderately high temperatures to support autotrophic growth (Mangold et al, 2011; Chen et al, 2012). It is the primary member of a consortium of sulfur oxidizers in different toxic-laden acidic environments, which are termed “extreme environments,” including coal pile and spoil, gold-bearing reactor operation, as well as low-grade copper bioleaching heap (Valdes et al, 2009; You et al, 2011; Zhang et al, 2016c). Research focusing on the correlation between genomic changes and evolutionary adaptation is of great interest

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