Proteomic signatures of cold adaptation and sponge host adaptation in marine Archaea

Temperature shapes the biochemistry of microbial proteins, and several amino acid compositional indices have been proposed to detect cold adaptation in microbial proteomes. Whether these indices capture cold adaptation in Archaea, which are abundant in cold marine environments such as the Arctic Ocean, has not been tested. We calculated six amino acid compositional indices (arginine to lysine ratio, acidic residue proportion, aliphatic index, aromaticity, grand average of hydropathicity, and proline residue proportion) across global protein families for 142 Marine Group I (MG-I; Thaumarchaeota) and 146 Euryarchaeota genomes from the Bacterial and Viral Bioinformatics Resource Center (BV-BRC), together with three MG-I metagenome-assembled genomes (MAGs) recovered from the Western Arctic Ocean. The Arctic MAGs fell within the range of index and phylogenetic distances of the wider MG-I population, and no signature of cold adaptation was detected. Instead, index values differed between the two main MG-I phylogenetic groups and between freshwater and marine genomes, and the Euryarchaeota formed five index-based clusters consistent with phylogeny. A group of 19 MG-I MAGs associated with sea sponges had significantly higher arginine to lysine ratios than other MG-I, differed in the usage of all amino acids except alanine and lysine, and had distinct codon usage and higher GC content; their anomalous placement in the MG-I phylogeny is consistent with long-branch attraction. These results indicate that amino acid compositional indices developed for Bacteria have limited power to detect cold adaptation in Archaea, but reveal strong proteomic signatures associated with host adaptation in sponge-associated Thaumarchaeota.