Insights into the genomic and metabolic adaptations of Termite Associated Verrucomicrobia strains using functional and comparative genomics
Abstract
The symbiotic gut organisms of termites play an important role in lignocellulose digestion and other related metabolic processes. Previous studies on Diplosphaera colitermitum TAV2, a Verrucomicrobium isolated from the hindgut of Reticulitermes flavipes, revealed its microaerophilic nature and involvement in important ecophysiological processes in the termite gut. In the present study, a detailed account of genomic sequences of 3 additional strains is provided, and the genomes of all 5 TAV strains isolated so far are compared, to gain a comprehensive understanding of these organisms. Our comparative genomic study shows that these strains represent two distinct species, and despite significant number of genes being conserved across the genomes, synteny of genomes between species is lost. We found important ecological attributes like microaerophilic physiology and the ability to digest lignocellulose to be conserved at the genomic level in these strains, suggesting their common roles in O2 scavenging and lignocellulose digestion. However, high numbers of genes associated with functional category transcription were present in species-specific genomes, suggesting differential regulation of gene expression to be a potential primary feature distinguishing these otherwise highly similar genomes. Our study identified signatures of adaptive variation in enzymes of the electron transport chain, which might be linked to microaerophilic physiology. Additionally, several membrane proteins/enzymes involved in recombination and repair, nitrogen metabolism and lignocellulose degradation were found undergoing adaptive evolution, reflecting the evolutionary mechanisms used by TAV strains to survive in the termite gut. Furthermore, the transcriptome of strain TAV2 under aerobic (20% O2) and hypoxic conditions (2% O2) was studied to understand its microaerophilic physiology. Putative CAZymes that degrade lignocellulose and other polysaccharides like pectin represent the majority of up-regulated genes. Genes associated with functional categories like oxidative stress protection, motility, amino acid metabolism, coenzyme metabolism were down-regulated. Additionally, changes in electron transport chain and putative oxygen sensing signal transducing proteins in the TAV2 strain were identified. In addition to corroborating our previous findings, these results reveal the metabolic adaptations used by TAV2 to survive in hypoxic conditions, and will serve as a foundation for future studies to understand the microaerophilic physiology of TAV strains.