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Genome Biol Evol. 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.

Author information

1
Sorbonne Universités, UPMC Univ. Paris 06, CNRS UMR 7144, Adaptation et Diversité en Milieu Marin, Equipe ABICE, Station Biologique de Roscoff, 29688 Roscoff, France.
2
Laboratory of Protein Physics, Institute of Protein Research, RAS, Institutskaya street, 4, 142290 Pushchino, Moscow, Russia.
3
CSTB - ICUBE, UMR7357, Faculté de Médecine, 4 rue Kirschleger, 67085 Strasbourg, France.
4
Department of Organismic & Evolutionary Biology, Harvard University Biological Laboratories, Cambridge, MA.

Abstract

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

PMID:
28082607
PMCID:
PMC5381640
DOI:
10.1093/gbe/evw298
[Indexed for MEDLINE]
Free PMC Article

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