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

Abstract

Background: Prokaryotic 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.

Results: Phylogenetic 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.

Conclusions: The 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).

Figure 1

Phylogenetic relationships among Pyrococcus strains (from [3-5,8,16,70-82]) based on the 16S rRNA gene sequences. Bayesian posterior probabilities of nodes are shown.

Figure 2

Phylogenetic relationships among the P. abyssi, P. horikoshii, P. furiosus, and T. onnurineus genomes based on the concatenated amino acid sequences. Bayesian posterior probabilities of nodes are shown. Ingroup branches are labeled a through d.

Figure 3

Number of gene clusters for which positive selection was detected by different approaches and different amino acid physicochemical categorizations. The bar colors for different approaches are shown on the right; y-axis: number of clusters; x-axis: branches (designations are as in Figure 2).

Figure 4

The values of the ν parameter reflecting changes in amino acid frequencies for different evolutionary tree branches for categorizations based on the van der Waals volume, hydropathy and isoelectric point. y-axis, amino acid groups (see Table 4); x-axis, v (see Methods section); branches are labeled as in Figure 2. Property designations: A, van der Waals volume; B, hydropathy; C, isoelectric point.

Figure 5

The values of the ν parameter reflecting changes in amino acid frequencies for different evolutionary tree branches for categorizations based on the physico-chemical properties combinations. Designations are as in Figure 4. Combination: A, polarity and hydropathy; B, polarity and volume; C, hydrophilicity and pressure asymmetry index; D, polarity and hydrophilicity.