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. 2017 Feb 1;9(2):279-296.
doi: 10.1093/gbe/evw298.

Proteome Evolution of Deep-Sea Hydrothermal Vent Alvinellid Polychaetes Supports the Ancestry of Thermophily and Subsequent Adaptation to Cold in Some Lineages

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Proteome Evolution of Deep-Sea Hydrothermal Vent Alvinellid Polychaetes Supports the Ancestry of Thermophily and Subsequent Adaptation to Cold in Some Lineages

Eric Fontanillas et al. Genome Biol Evol. .
Free PMC article


Temperature, perhaps more than any other environmental factor, is likely to influence the evolution of all organisms. It is also a very interesting factor to understand how genomes are shaped by selection over evolutionary timescales, as it potentially affects the whole genome. Among thermophilic prokaryotes, temperature affects both codon usage and protein composition to increase the stability of the transcriptional/translational machinery, and the resulting proteins need to be functional at high temperatures. Among eukaryotes less is known about genome evolution, and the tube-dwelling worms of the family Alvinellidae represent an excellent opportunity to test hypotheses about the emergence of thermophily in ectothermic metazoans. The Alvinellidae are a group of worms that experience varying thermal regimes, presumably having evolved into these niches over evolutionary times. Here we analyzed 423 putative orthologous loci derived from 6 alvinellid species including the thermophilic Alvinella pompejana and Paralvinella sulfincola. This comparative approach allowed us to assess amino acid composition, codon usage, divergence, direction of residue changes and the strength of selection along the alvinellid phylogeny, and to design a new eukaryotic thermophilic criterion based on significant differences in the residue composition of proteins. Contrary to expectations, the alvinellid ancestor of all present-day species seems to have been thermophilic, a trait subsequently maintained by purifying selection in lineages that still inhabit higher temperature environments. In contrast, lineages currently living in colder habitats likely evolved under selective relaxation, with some degree of positive selection for low-temperature adaptation at the protein level.

Keywords: RNAseq; hydrothermal vents; protein composition; selection; thermal adaptation.


<sc>Fig</sc>. 1.—
Fig. 1.—
Main prokaryotic thermophilic amino acid indices (IVYWREL, EK/QH, and CvP_bias criteria) in “hot” and “cold” alvinellid species using translated sequences of 423 orthologous transcripts. (a) Overall CvP_bias between species, (b) overall EK/QH vs. IVYWREL biplot between species.
<sc>Fig</sc>. 2.—
Fig. 2.—
Factorial correspondence analysis of the amino acid frequencies between protein orthologous sequences of six alvinellid species.
<sc>Fig</sc>. 3.—
Fig. 3.—
Unrooted phylogenomic ML tree of alvinellids with patristic distances (in bold). All nodes were fully supported by 100% bootstrap values.
<sc>Fig</sc>. 4.—
Fig. 4.—
Factorial correspondence analysis (FCA) of orientated amino acid substitution frequencies between orthologous protein sequences of alvinellid species. The dashed envelope represents the cloud of remaining substitution points.
<sc>Fig</sc>. 5.—
Fig. 5.—
Derived amino acid replacement rates and median intergenes dN/dS ratios observed on the terminal branches of the tree. Each rate was weighted with the length (t) of the corresponding terminal branch obtained after tree ultrametrization. Absolute timing inferred under a clock hypothesis on the mt Cox1 gene (see supplementary fig. S1, Supplementary Material online) and its evolutionary rate estimated from Chevaldonné et al. (2002) produced exactly the same results. The null hypothesis of constant rate of derived replacements was rejected using a χ 2 test (χ 2 =1326, dfl = 5). (a) Derived mutation rates, (b) dN/dS ratios in terminal branches, (c) P-values represent the level of dN/dS significance following an ecological a priori Binomial test (i.e. values of a given species significantly greater or lower than either “cold” (§) or “hot” (#) species).
<sc>Fig</sc>. 6.—
Fig. 6.—
Biplot of dN/dS versus dS medians obtained over branches of the phylogenomic ML tree of the six alvinellid species with the free-ratio branch-model M1 implemented in PaML 4.0 (Yang 2007). Branch values are significantly (P < 0.01: Pearson’s r test) linearly regressed without using the branch leading to Alvinella spp. (outside of the confidence envelope at 95% for the whole dataset).
<sc>Fig</sc>. 7.—
Fig. 7.—
Ancestral reconstruction of amino acid changes using the alvinellid criteria PAYLE vs. DGMS along the phylogenomic tree of alvinellid worms following the Bayesian reconstruction of ancestral sequences implemented in aaML of PaML (Yang 2007).

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