Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

Abstract

Recent phylogenomic analysis has suggested that three strains isolated from different copper mine tailings around the world were taxonomically affiliated with Sulfobacillus thermosulfidooxidans. Here, we present a detailed investigation of their genomic features, particularly with respect to metabolic potentials and stress tolerance mechanisms. Comprehensive analysis of the Sulfobacillus genomes identified a core set of essential genes with specialized biological functions in the survival of acidophiles in their habitats, despite differences in their metabolic pathways. The Sulfobacillus strains also showed evidence for stress management, thereby enabling them to efficiently respond to harsh environments. Further analysis of metabolic profiles provided novel insights into the presence of genomic streamlining, highlighting the importance of gene loss as a main mechanism that potentially contributes to cellular economization. Another important evolutionary force, especially in larger genomes, is gene acquisition via horizontal gene transfer (HGT), which might play a crucial role in the recruitment of novel functionalities. Also, a successful integration of genes acquired from archaeal donors appears to be an effective way of enhancing the adaptive capacity to cope with environmental changes. Taken together, the findings of this study significantly expand the spectrum of HGT and genome reduction in shaping the evolutionary history of Sulfobacillus strains.IMPORTANCE Horizontal gene transfer (HGT) and gene loss are recognized as major driving forces that contribute to the adaptive evolution of microbial genomes, although their relative importance remains elusive. The findings of this study suggest that highly frequent gene turnovers within microorganisms via HGT were necessary to incur additional novel functionalities to increase the capacity of acidophiles to adapt to changing environments. Evidence also reveals a fascinating phenomenon of potential cross-kingdom HGT. Furthermore, genome streamlining may be a critical force in driving the evolution of microbial genomes. Taken together, this study provides insights into the importance of both HGT and gene loss in the evolution and diversification of bacterial genomes.

Codon usage bias reveals genomic adaptations to environmental conditions in an acidophilic consortium

“…These extreme conditions induce selective pressures which have an impact on indigenous organisms, for example, the principal acidophilic organisms are autotrophic, able to use ferrous iron and reduced sulfur compounds as electron donors which are released from sulfide minerals during oxidative dissolution [ 8 ]. Apart from nutritional selection, it is plausible to hypothesize that genes from such organisms have also been genetically selected in order to improve the ability of the organism to survive under extreme conditions [ 49 ].…”

Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing

“…They are lost and gained more readily than core genes [ 25 – 27 ], and can endow their recipient with new traits that facilitate adaptation to a changing environment [ 28 , 29 ]. For example, the horizontal transfer of such genes has helped marine microbes adapt to a variety of carbon sources [ 19 , 30 ], it has helped bacteria adapt to extreme environments [ 31 , 32 ], and it has helped gut microbial communities or pathogens adapt to human hosts [ 33 , 34 ]. A recent comparative studies of 53 E. coli genomes showed that at least 10% of adaptations to new environments may have been achieved by horizontal gene transfer [ 35 ].…”

Pan-Genome Analysis Links the Hereditary Variation of Leptospirillum ferriphilum With Its Evolutionary Adaptation

“…The emergence of next generation sequencing technologies accompanied with developing methodological and computational approaches has yielded valuable insights into the genetic traits of microorganisms in various habitats worldwide, such as their metabolic capabilities and evolutionary adaptation ( Cordero and Polz, 2014 ; Ji et al, 2014 ; Zhang and Sievert, 2014 ; Youssef et al, 2015 ; Zhang et al, 2016a , b , e , 2017a ). Plentiful genome data deluge in public databases have fueled the field of comparative genomics.…”

“…Studies on bacterial genomes significantly expanded the scope of inter-species divergence ( Ullrich et al, 2016 ; Zhang et al, 2016e ). Also, intra-species differentiation has been observed based on individual genomes of certain species ( Zhang et al, 2016a , b , 2017a ). Spatial distance and environmental heterogeneity are recognized to be two major factors that contribute to genetic variation of microbial genomes and populations ( Ramette and Tiedje, 2007 ).…”