High temperature deep-sea vents support a rich phylogenetic and physiological diversity of thermophilic Bacteria and Archaea. Like in other ecosystems, the advent of 16S rRNA amplicon sequencing revealed how diverse the hydrothermal communities are and how many lineages have very few, if any, representatives in culture (Flores et al., 2011, Flores et al., 2012). For example, most of the characterized isolated archaeal cultures from deep-sea vents are Methanobacteriota, Thermoplasmatota and Halobacteriota (all syn. Euryarchaeota; Chuvochina et al., 2023), yet from amplicon sequencing, the Thermoproteota (syn. Crenarchaeota) are much more prevalent and more phylogenetically diverse than previously assumed. Further, the diversity and relative abundance of some community members from the Thermoproteota helped drive differences in the observed microbial community structures at Lucky Strike vent field versus Rainbow vent field along the Mid-Atlantic Ridge (Flores et al., 2011). The Thermoproteota are also noticeably underrepresented in genomic databases.

Within the Thermoproteota, prevalent orders associated with deep-sea vents (e.g. Flores et al., 2011, Flores et al., 2012, Zhou et al., 2022) include the Thermofilales (e.g. Thermofilum), Thermoproteales (e.g. Pyrobaculum), and the Desulfurococcales (includes the Pyrodictiaceae, Desulfurococcaceae families, e.g. Desulfurococcus, Aeropyrum, Pyrodictium). Metabolically, the Desulfurococcales are very diverse, encompassing the range of autotrophs (e.g. Ignicoccus; Huber et al., 2000, Paper et al., 2007) heterotrophs (e.g. Desulfurococcus, Ignisphaera; Niederberger et al., 2006, Zillig et al., 1982), aerobes (e.g. Aeropyrum; Nakagawa et al., 2004, Sako et al., 1996) anaerobes (e.g. Desulfurococcus, Thermodiscus; Stetter, 2001, Zillig et al., 1982), fermenters (e.g. Hyperthermus, Ignisphaera; Niederberger et al., 2006, Zillig et al., 1991) and nitrate (e.g. Pyrodictium; Lin et al., 2016), sulfur (e.g. Thermodiscus; Stetter, 2001), iron (e.g. Pyrodictium; Lin et al., 2016), thiosulfate (e.g. Zestosphaera; St. John et al., 2019a) and perchlorate (e.g. Aeropyrum; Liebensteiner et al., 2015) respirers. Some also serve as hosts (e.g. Ignicoccus, Zestosphaera; Huber et al., 2002, St. John et al., 2019a) for the Nanobdellota (syn. Nanoarchaeota; Kato et al., 2022).

Taxonomically, considerable uncertainty exists within the Desulfurococcales as phylogenetic trees based on 16S rRNA gene sequences are often polyphyletic (Boyd et al., 2007, Jay et al., 2014, Niederberger et al., 2006, Prokofeva et al., 2000). In particular, the phylogenetic placement of members of the Desulfurococcaceae family has illustrated some of the taxonomic issues in this ecologically important group of Archaea. As more 16S rRNA genes have been sequenced, some incongruencies have emerged within the phylogeny of this family, namely the unstable position of the Aeropyrum-Thermodiscus-Stetteria clade. As genomes and metagenome assembled genomes (MAGs) have been added to the phylogenomic framework of the family however, more robust support for these issues has been realized, and whole genome analysis places this clade and Caldisphaera firmly within the family Acidilobaceae (Prokofeva et al., 2009), which is mostly represented by acid-tolerant thermophilic isolates from terrestrial hot springs (Boyd et al., 2007, Prokofeva et al., 2000, Prokofeva et al., 2009). While the Genome Taxonomy Database (GTDB) further illuminated these issues by classifying this clade within the Acidilobaceae, no formal proposal has been published for including previously classified Caldisphaeraceae and Desulfurococcaceae into the Acidilobaceae. Using an extensive MAG dataset from deep-sea hydrothermal vents, we demonstrate that Aeropyrum, Thermodiscus, Caldisphaera and their relatives form a monophyletic clade with members of the Acidilobaceae. Here, we propose amending the description of the Acidilobaceae to include these Desulfurococcaceae and the Caldisphaeraceae and propose several new genera in this family based on high quality MAGs and metabolic criteria.