Proteome evolution of deep-sea hydrothermal vent alvinellid polychaetes supports the ancestry of thermophily and subsequent adaptation to cold in some lineages

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.

Spaghetti to a Tree: A Robust Phylogeny for Terebelliformia (Annelida) Based on Transcriptomes, Molecular and Morphological Data

“…The transcriptomic and Sanger sequences found that Paralvinella is paraphyletic owing to the position of Alvinella. This has been suggested based on a previous study using transcriptomic data, where Alvinella and Paralvinella were not reciprocally monophyletic in all gene trees [69], but an outgroup was missing to fully interpret these results. Here, we showed unequivocally that Paralvinella pandorae and P. irlandei were a sister group to Alvinella and the other Paralvinella species and so should be referred to Nautalvinella, originally a subgenus of Paralvinella that was erected based on gill morphology [70].…”

Heritable pattern of oxidized DNA base repair coincides with pre-targeting of repair complexes to open chromatin

“…Given the key and prototypical role of AcNEIL1 in genome repair, we examined the evolutionary conservation of Neil1 and its acetylation center in the two main lineages of bilateria (560–0 Ma), deuterostomes and protostomes. We included the sequence of the polychaete worm A. pompejana , an ancestral extremophile residing in deep-sea hydrothermal vents ( 48 ), which we obtained from partial genome assembly from specimens collected during an expedition on the East Pacific Rise ( Supplementary Figure S10A ). A total of 241/260 species comprising all deuterostomes (540–0 Ma) and Lophotrochozoa (536–0 Ma), and part of the Ecdysozoa clade displayed strong evolutionary conservation (blastp values between 7e −64 and 33 −112 ), although no significant hits were found in Nematoda and Hexapoda, which include the model genomes of Caenorhabditis elegans and Drosophila melanogaster (Figure 6A ).…”

Comparative transcriptome analysis reveals potential evolutionary differences in adaptation of temperature and body shape among four Percidae species

“…For examples, similar researches were performed on cactophilic Drosophila , and the Tibetan fish Gymnodiptychus pachycheilus to identify potential candidate genes for environmental adaptation [68, 69]. Similarly, comparative transcriptome analysis in alvinellid polychaetes revealed that the trait of thermophilic species that still inhabit higher temperature environments was maintained by purifying selection in lineages, while the trait of lineages currently living in colder habitats was likely obtained under selective relaxation, with some degree of positive selection for low-temperature adaptation at the protein level [70].…”