Molecular evolution of the hyperthermophilic archaea of the Pyrococcus genus: analysis of adaptation to different environmental conditions

Abstract

BackgroundProkaryotic microorganisms are able to survive and proliferate in severe environmental conditions. The increasing number of complete sequences of prokaryotic genomes has provided the basis for studying the molecular mechanisms of their adaptation at the genomic level. We apply here a computer-based approach to compare the genomes and proteomes from P. furiosus, P. horikoshii, and P. abyssi to identify features of their molecular evolution related to adaptation strategy to diverse environmental conditions.ResultsPhylogenetic analysis of rRNA genes from 26 Pyrococcus strains suggested that the divergence of P. furiosus, P. horikoshii and P. abyssi might have occurred from ancestral deep-sea organisms. It was demonstrated that the function of genes that have been subject to positive Darwinian selection is closely related to abiotic and biotic conditions to which archaea managed to become adapted. Divergence of the P. furiosus archaea might have been due to loss of some genes involved in cell motility or signal transduction, and/or to evolution under positive selection of the genes for translation machinery. In the course of P. horikoshii divergence, positive selection was found to operate mainly on the transcription machinery; divergence of P. abyssi was related with positive selection for the genes mainly involved in inorganic ion transport. Analysis of radical amino acid replacement rate in evolving P. furiosus, P. horikoshii and P. abyssi showed that the fixation rate was higher for radical substitutions relative to the volume of amino acid side-chain.ConclusionsThe current results give due credit to the important role of hydrostatic pressure as a cause of variability in the P. furiosus, P. horikoshii and P. abyssi genomes evolving in different habitats. Nevertheless, adaptation to pressure does not appear to be the sole factor ensuring adaptation to environment. For example, at the stage of the divergence of P. horikoshii and P. abyssi, an essential evolutionary role may be assigned to changes in the trophic chain, namely, acquisition of a consumer status at a high (P. horikoshii) or low level (P. abyssi).

Comparative Analysis of Barophily-Related Amino Acid Content in Protein Domains ofPyrococcus abyssiandPyrococcus furiosus

“…The cumulative plot of species-specific FSFs for the two Pyrococci indicates early divergence both in structure and in function. This result is congruent with other studies that suggest early divergence based on sequence phylogeny and gene loss [19] and a very ancestral trend of loss in protein domain repertoires of Archaea responsible for their very early origin [16]. Since the age of FSF domain structures follows a tight molecular clock [20], it was possible to establish a timeframe for the appearance of lineage-specific FSFs in evolution.…”

“…P. abyssi has fewer FSFs (472) than P. furiosus (495), probably because it inhabits an extremophilic niche that combines extreme pressure and temperature, both of which have been shown to put limits on viable protein structures (e.g., [23, 24]). The similarities in FSF content of proteomes are explained by the common biological heritage and similar physiology of the two organisms, which differ mainly in the utilization of metabolic substrates [19]. These differences must be reflected in the function of FSFs that are specific to each of the two organisms.…”

“…Thus, it is likely that the bias in the amino acid composition of protein sequences is reflected in protein structure, which could allow the study of the evolutionary divergence of organisms from a common thermo-barophilic ancestor. The hyper thermophilic barophile Pyrococcus abyssi and hyper thermophilic nonbarophile P. furiosus are two closely related organisms that are very suitable for such analysis due to the extreme similarity of their physiology [19] and the very early evolutionary origins of its lineages [16]. …”

Genome variation in the hyperthermophilic archaeonAeropyrum

“…2 Comparative genome analysis between closely related organisms shows relevant physiological differences depending on their habitat, which are reflected in genome divergence. 3,4 We recently determined the complete genome sequence of A. camini and compared it with the A. pernix genome 5 to determine the genetic differences between close relatives in distinct habitats. 6 The general genome features were similar between A. camini and A. pernix: small genome size (1.60 to 1.67 Mbp), G+C content (56.3 to 56.7%), and number of open reading frames (ORFs) (1645 to 1700).…”

Variation of the Virus-Related Elements within Syntenic Genomes of the Hyperthermophilic Archaeon Aeropyrum

“…For example, whole-genomic comparisons of the cyanobacterial Prochlorococcus spp., with physiological features relevant to the different ecological niches within a stratified oceanic water column, show gross signatures of this niche differentiation (1). The members of the anaerobic hyperthermophilic archaeal genus Pyrococcus adapt to abiotic and biotic environmental conditions through positive gene selection (2). Although genomes of temperate coastal SAR11 isolates are highly conserved in the core genome common to all strains (3) and show synteny (the conservation of DNA sequence and gene order) (4), variations exist among genes for phosphorus metabolism, glycolysis, and C 1 metabolism.…”