Despite their discovery over 25 years ago, the Marine Group II Euryarchaea (MGII) have remained a difficult group of organisms to study, lacking cultured isolates and genome references. The MGII have 10 been identified in marine samples from around the world and evidence supports a photoheterotrophic lifestyle combining phototrophy via proteorhodopsins with the remineralization of high molecular weight organic matter. Divided between two Orders, the MGII have distinct ecological patterns that are not understood based on the limited number of available genomes. Here, we present the comparative genomic analysis of 322 MGII genomes, providing the most detailed view of these mesophilic archaea to-date. 15This analysis identified 17 distinct Family level clades including nine clades that previously lacked reference genomes. The metabolic potential and ecological distribution of the MGII genera revealed distinct roles in the environment, identifying algal-saccharide-degrading coastal genera, protein-degrading oligotrophic surface ocean genera, and mesopelagic genera lacking proteorhodopsins common in all other families. This study redefines the MGII and provides an avenue for understanding the role these 20 organisms play in the cycling of organic matter throughout the water column.
Main textSince their discovery by DeLong 1 (1992), despite global distribution and representing a significant portion of the microbial plankton in the photic zone, the Marine Group II (MGII) Euryarchaea 25have remained an enigmatic group of organisms in the marine the environment. The MGII have been predominantly identified in the surface oceans 2 , account for ~15% of the archaeal cells in the oligotrophic open ocean 3 , and shown to increase in abundance in response to phytoplankton blooms 4 comprising up to ~30% of the total microbial community 5 . Research has shown that the MGII correspond with specific genera of phytoplankton 6 , during and after blooms 7 , and can be associated with particles when samples 30 are size fractionated 8 . Phylogenetic analyses have revealed the presence of two dominant clades of MGII, referred to as MGIIA and MGIIB (the MGIIB have recently been named Thalassoarchaea 9 ), that respond to different environmental conditions, including temperature and nutrients 10 . To date, the MGII have not been successfully cultured or enriched from the marine environment. Instead our current understanding of the role these organisms play in the environment is derived from 35interpretations of ecological data (i.e., phytoplankton-and particle-associated) and a limited number of genomic fragments and reconstructed environmental genomes. Collectively, these genomic studies have revealed a number of re-occurring traits common to the MGII, including: proteorhodopsins in MGII sampled from the photic zone 11 , genes targeting the degradation of high molecular weight (HMW) organic matter, such as proteins, carbohydrates, and lipids, and subsequent transport of constituent 40 components into the cell 9,12-14 , genes representative...