Genome Implosion Elicits Host-Confinement in Alcaligenaceae: Evidence from the Comparative Genomics of Tetrathiobacter kashmirensis, a Pathogen in the Making

Abstract

This study elucidates the genomic basis of the evolution of pathogens alongside free-living organisms within the family Alcaligenaceae of Betaproteobacteria. Towards that end, the complete genome sequence of the sulfur-chemolithoautotroph Tetrathiobacter kashmirensis WT001T was determined and compared with the soil isolate Achromobacter xylosoxidans A8 and the two pathogens Bordetella bronchiseptica RB50 and Taylorella equigenitalis MCE9. All analyses comprehensively indicated that the RB50 and MCE9 genomes were almost the subsets of A8 and WT001T, respectively. In the immediate evolutionary past Achromobacter and Bordetella shared a common ancestor, which was distinct from the other contemporary stock that gave rise to Tetrathiobacter and Taylorella. The Achromobacter-Bordetella precursor, after diverging from the family ancestor, evolved through extensive genome inflation, subsequent to which the two genera separated via differential gene losses and acquisitions. Tetrathiobacter, meanwhile, retained the core characteristics of the family ancestor, and Taylorella underwent massive genome degeneration to reach an evolutionary dead-end. Interestingly, the WT001T genome, despite its conserved architecture, had only 85% coding density, besides which 578 out of its 4452 protein-coding sequences were found to be pseudogenized. Translational impairment of several DNA repair-recombination genes in the first place seemed to have ushered the rampant and indiscriminate frame-shift mutations across the WT001T genome. Presumably, this strain has just come out of a recent evolutionary bottleneck, representing a unique transition state where genome self-degeneration has started comprehensively but selective host-confinement has not yet set in. In the light of this evolutionary link, host-adaptation of Taylorella clearly appears to be the aftereffect of genome implosion in another member of the same bottleneck. Remarkably again, potent virulence factors were found widespread in Alcaligenaceae, corroborating which hemolytic and mammalian cell-adhering abilities were discovered in WT001T. So, while WT001T relatives/derivatives in nature could be going the Taylorella way, the lineage as such was well-prepared for imminent host-confinement.

Survival of taylorellae in the environmental amoeba Acanthamoeba castellanii

“…On the other hand, no amoeba-related genes were identified during the analysis of taylorellae genomes [ 10 , 12 ]. This observation seems coherent with the plausible evolutionary path of taylorellae reported by Gosh et al, [ 13 ] which suggests that the evolution of the taylorellae genome is mainly based on a reduction in size, with very few new gene acquisitions since taylorellae’s separation from the last Alcaligenaceae common ancestor [ 13 ].…”

“…The recently-described taylorellae MultiLocus Sequence Typing (MLST) scheme, which reveals the highly clonal dissemination of taylorellae (especially T. equigenitalis ), combined with the emergence of new STs over time suggest that Equidae could be contaminated by an external source of Taylorella originating from an as yet unidentified natural ecological reservoir. Moreover, genome sequence analysis of Alcaligenaceae members suggests that taylorellae diverged by genome reduction from an ancestor which probably had a less specific ecological niche [ 13 ] than present day Taylorellae.…”

Role of Gut Dysbiosis in Liver Diseases: What Have We Learned So Far?

“…Ahluwalia et al [205] reported that fecal Enterobacteriaceae was positively correlated and autochthonous taxa was negatively correlated with hyperammonemia-associated astrocytic changes on magnetic resonance spectroscopy and that Porphyromonadaceae was correlated with neuronal changes on diffusion tensor imaging. The relation of Enterobacteriaceae and Alcaligeneceae to HE may be partly explained by the fact that these bacteria degrade urea to produce ammonia [188,206,207]. In addition, Enterobacteriaceae is a known organism that produces potent endotoxin.…”

The host model Galleria mellonella is resistant to taylorellae infection

“…These observations support the hypothesis stated by Ghosh et al . () that the taylorellae genome has suffered a drastic decline in size, leading to a limited survival capacity and a specialized ecological niche. The absence of manifested virulence by taylorellae and the rapid elimination of taylorellae from G. mellonella larvae supports the hypothesis that taylorellae pathogenicity depends on species‐specific requirements to establish an infection.…”