Chromosome-scale genome assembly and gene annotation of the hydrothermal vent annelid Alvinella pompejana yield insight into animal evolution in extreme environments.

Abstract

Background: The Pompeii worm Alvinella pompejana, a terebellid annelid, has long been an exemplar of a metazoan that lives in an extreme environment, on the chimney wall of deep-sea hydrothermal vents, but this very environment has made it difficult to study. Comprehensive assessment of Alvinella pompejana genome content, and the factors that could explain its ability to thrive in seemingly hostile conditions has been lacking.

Results: We report the chromosome-level genome sequence of Alvinella pompejana and population-level sequence variants. We produced a set of gene models and analysed the predicted protein set in the light of past hypotheses about the thermotolerance of Alvinella, comparing it to other recently sequenced vent annelids. Despite its extreme environment, we find evidence for relatively conservative evolution of protein amino acid composition and genome evolution as measured by synteny. We suggest that prior hypotheses of loss of amino acid biosynthesis genes associated with obligate symbioses reported in siboglinid annelids are mistaken, and that Alvinella and siboglinids are typical metazoans in this regard. Alvinella encodes a number of respiratory enzymes unusual for bilaterian animals, suggesting an ability to better tolerate hypoxic environments. We find evidence of a parallel increase in the number of globin encoding genes and loss of light sensitive opsins and cryptochromes in deep-sea annelids.

Conclusions: Our results provide a comprehensive Alvinella protein and genome resource and shed light on the adaptation of Alvinella to temperature, hypoxia and darkness, as well as cryptic speciation, giving a firm base from which future studies can be taken forward.