Comparative Genomics of Extremophile Archaea from Deep-Sea Hydrothermal Vents
DOI:
https://doi.org/10.5281/zenodo.22687972Keywords:
archaea, hydrothermal vents, comparative genomics, extremophiles, horizontal gene transfer, thermal adaptationAbstract
Deep-sea hydrothermal vents host archaeal communities that grow at temperatures, pressures and chemical
extremes that would be lethal to nearly all other life, and their genomes are expected to carry the molecular
signatures of that adaptation in ways that remain incompletely catalogued outside a small number of well-studied
model lineages. We assembled and compared 34 metagenome-assembled genomes (MAGs) recovered from
black smoker chimney and diffuse-flow sediment samples collected at three hydrothermal vent fields (Mid-Atlantic
Ridge, East Pacific Rise, and Mariana back-arc), spanning the phyla Crenarchaeota, Euryarchaeota,
Thaumarchaeota and the more recently described Asgard superphylum, against a reference set of 156 publicly
available archaeal genomes from non-vent environments. Vent-associated archaea showed significant
enrichment, relative to the non-vent reference set, in genes encoding reverse gyrase (present in 97% of vent
MAGs versus 34% of non-vent genomes, chi-squared P<0.001), a topoisomerase strongly associated with growth
above 80C, and in genes encoding di- and tri-ether membrane lipid biosynthesis enzymes associated with
membrane stability at high temperature. Comparative analysis of amino acid composition across 1,842
single-copy orthologous proteins found consistent enrichment of charged and hydrophobic residues at the
expense of polar uncharged residues in vent-associated lineages, a pattern previously linked to protein
thermostability in laboratory-characterised hyperthermophiles. Network analysis of predicted horizontal gene
transfer events identified a disproportionate number of transfers involving genes for metal resistance and sulfur
metabolism clustering by vent field rather than by phylogenetic lineage, consistent with local environmental
selection acting across lineage boundaries at each vent site independently. These results extend genomic
evidence for thermal and chemical adaptation beyond the handful of cultured hyperthermophile model organisms
to a broader, largely uncultured diversity of vent-associated archaea, and identify site-specific horizontal gene
transfer as an underappreciated contributor to local adaptation at individual vent fields.
Keywords: Deep-sea hydrothermal vents host archaeal communities that grow at temperatures, pressures and chemical
extremes that would be lethal to nearly all other life, and their genomes are expected to carry the molecular
signatures of that adaptation in ways that remain incompletely catalogued outside a small number of well-studied
model lineages. We assembled and compared 34 metagenome-assembled genomes (MAGs) recovered from
black smoker chimney and diffuse-flow sediment samples collected at three hydrothermal vent fields (Mid-Atlantic
Ridge, East Pacific Rise, and Mariana back-arc), spanning the phyla Crenarchaeota, Euryarchaeota,
Thaumarchaeota and the more recently described Asgard superphylum, against a reference set of 156 publicly
available archaeal genomes from non-vent environments. Vent-associated archaea showed significant
enrichment, relative to the non-vent reference set, in genes encoding reverse gyrase (present in 97% of vent
MAGs versus 34% of non-vent genomes, chi-squared P<0.001), a topoisomerase strongly associated with growth
above 80C, and in genes encoding di- and tri-ether membrane lipid biosynthesis enzymes associated with
membrane stability at high temperature. Comparative analysis of amino acid composition across 1,842
single-copy orthologous proteins found consistent enrichment of charged and hydrophobic residues at the
expense of polar uncharged residues in vent-associated lineages, a pattern previously linked to protein
thermostability in laboratory-characterised hyperthermophiles. Network analysis of predicted horizontal gene
transfer events identified a disproportionate number of transfers involving genes for metal resistance and sulfur
metabolism clustering by vent field rather than by phylogenetic lineage, consistent with local environmental
selection acting across lineage boundaries at each vent site independently. These results extend genomic
evidence for thermal and chemical adaptation beyond the handful of cultured hyperthermophile model organisms
to a broader, largely uncultured diversity of vent-associated archaea, and identify site-specific horizontal gene
transfer as an underappreciated contributor to local adaptation at individual vent fields.
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