Interplay of Various Evolutionary Modes in Genome Diversification and Adaptive Evolution of the Family Sulfolobaceae.

Rachana Banerjee,Abhishake Lahiri,Chitra Dutta,Daniel H Huson,Sandip Paul,Anupam Gautam,Narendrakumar M Chaudhari,Sujay Chattopadhyay,Debaleena Bhowmik

doi:10.3389/fmicb.2021.639995

Abstract

Sulfolobaceae family, comprising diverse thermoacidophilic and aerobic sulfur-metabolizing Archaea from various geographical locations, offers an ideal opportunity to infer the evolutionary dynamics across the members of this family. Comparative pan-genomics coupled with evolutionary analyses has revealed asymmetric genome evolution within the Sulfolobaceae family. The trend of genome streamlining followed by periods of differential gene gains resulted in an overall genome expansion in some species of this family, whereas there was reduction in others. Among the core genes, both Sulfolobus islandicus and Saccharolobus solfataricus showed a considerable fraction of positively selected genes and also higher frequencies of gene acquisition. In contrast, Sulfolobus acidocaldarius genomes experienced substantial amount of gene loss and strong purifying selection as manifested by relatively lower genome size and higher genome conservation. Central carbohydrate metabolism and sulfur metabolism coevolved with the genome diversification pattern of this archaeal family. The autotrophic CO2 fixation with three significant positively selected enzymes from S. islandicus and S. solfataricus was found to be more imperative than heterotrophic CO2 fixation for Sulfolobaceae. Overall, our analysis provides an insight into the interplay of various genomic adaptation strategies including gene gain–loss, mutation, and selection influencing genome diversification of Sulfolobaceae at various taxonomic levels and geographical locations.

Highlights

The microbial genome divergence is a dynamic evolutionary process of ecological and genetic differentiation
The internal or terminal nodes that were represented by either single strain or multiple strains of a particular species experienced an overall level of gene gain with one exception of S. acidocaldarius
Pan-genomics coupled with gene gain–loss analysis explored the inherent pattern of genome streamlining, followed by waves of differential gene gains, which resulted as genome expansion in some species while reduction in others in comparison to the ancestral state

Summary

Introduction

The microbial genome divergence is a dynamic evolutionary process of ecological and genetic differentiation Various mechanisms that both create and maintain the phenotypic diversity in genomes include gene gain–loss, mutation, natural selection, and genetic drift (Loewe and Hill, 2010). A considerable fraction of the genetic diversity is likely to be considered as regulators of adaptive features specific for that particular habitat Deciphering these adaptive signals encrypted in the genomes of any organism is important from both evolutionary and ecological perspectives. The complex nature of these signals due to the multilayer interactions either with cohabitants or with environment makes the task extremely challenging In this context, one important module of research is the evolutionary dynamics of extremophiles that offer insights into how their genome-wide variations, linked to structural and functional profiles, are shaped by extreme environmental attributes (Horikoshi and Grant, 1998; Seckbach, 2000). Several studies have reported on the influence of genomic attributes including relative synonymous codon usage bias, dinucleotide abundance, purine loading, and horizontal gene transfers (HGTs) on sustaining extreme conditions (Lynn et al, 2002; Das et al, 2006; Paul et al, 2008; Dutta and Paul, 2012; van Wolferen et al, 2013)

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