Elshahed, Mostafa S.

Abstract Krum.hol.zi.bac.te.ri.o'ta. N.L. neut. n. Krumholzibacterium , type genus of the type class of the phylum; L. neut. pl. n. suff. ‐ota , ending to denote a phylum; N.L. neut. pl. n. Krumholzibacteriota , the phylum of the class Krumholzibacteria. The phylum Candidatus Krumholzibacteriota was proposed to accommodate genomic assemblies of yet‐uncultured microorganisms. The type species, of the genus, Candidatus Krumholzibacterium zodletonense Zgenome0171 T was recovered from an anaerobic, sulfide‐ and sulfur‐rich spring in Southwestern Oklahoma, USA. The phylum comprises one described class, order, family, genus, and species. However, currently available genomes ( n  = 90) in GTDB (release 08‐RS214) are accommodated in 1 class, 6 orders, 8 families, 30 genera, and 58 species. Phylogenetically, the phylum is closely related to Gemmatimonadota and multiple phyla with no cultured representatives ( Ca . Edwardsbacteria, Ca . Eisenbacteria, Ca . Latescibacterota, Ca . Zixibacteria, 4572‐55, ARS69, GCA‐2686955, JAAXHH01, JABDJQ01, JAGLTZ01, JAGLYR01, TA06, TA06_A, and VGIX01); all of which are part of the FCB ( Fibrobacteres , Chlorobia , Bacteroidetes ) superphylum in the Gracilicutes clade. Candidatus Krumholzibacteriota genomes have mainly been recovered from marine, freshwater, engineered, and host‐associated ecosystems. The prevailing in‐situ conditions in sampled habitats, gene content analysis, and the use of predictive machine learning‐based approaches suggest a phylum‐wide preference for anaerobic conditions, mesophilic temperatures, circumneutral pH, and low salinities. Metabolically, the type species of the type genus of the phylum is predicted to be a fermentative anaerobe with preference for amino acids over sugars as substrates. Later studies indicate that some members of the phylum harbor respiratory capacities (dissimilatory sulfate reduction, dissimilatory sulfite reduction, iron‐reduction, and high‐affinity oxygen respiration with a few members possessing the potential for low‐affinity oxygen respiration), while others possess the machinery for anaerobic degradation of aromatic hydrocarbons. Finally, although all members of Candidatus Krumholzibacteriota remain uncultured, a representative of the phylum was enriched in a methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments. Type genus : Candidatus Krumholzibacterium Youssef et al. 2019, CL2.

Summary We report on the genomic characterization of three novel classes in the phylum Desulfobacterota. One class (proposed name Candidatus ‘Anaeroferrophillalia’) was characterized by heterotrophic growth capacity, either fermentatively or utilizing polysulfide, tetrathionate or thiosulfate as electron acceptors. In the absence of organic carbon sources, autotrophic growth via the Wood–Ljungdahl (WL) pathway and using hydrogen or Fe(II) as an electron donor is also inferred for members of the ‘Anaeroferrophillalia’. The second class (proposed name Candidatus ‘Anaeropigmentia’) was characterized by its capacity for growth at low oxygen concentration, and the capacity to synthesize the methyl/alkyl carrier CoM, an ability that is prevalent in the archaeal but rare in the bacterial domain. Pigmentation is inferred from the capacity for carotenoid (lycopene) production. The third class (proposed name Candidatus ‘Zymogenia’) was characterized by fermentative heterotrophic growth capacity, broad substrate range and the adaptation of some of its members to hypersaline habitats. Analysis of the distribution pattern of all three classes showed their occurrence as rare community members in multiple habitats, with preferences for anaerobic terrestrial, freshwater and marine environments over oxygenated (e.g. pelagic ocean and agricultural land) settings. Special preference for some members of the class Candidatus ‘Zymogenia’ for hypersaline environments such as hypersaline microbial mats and lagoons was observed.