Salam, Nimaichand

Abstract Background The Atribacterota are widely distributed in the subsurface biosphere. Recently, the first Atribacterota isolate was described and the number of Atribacterota genome sequences retrieved from environmental samples has increased significantly; however, their diversity, physiology, ecology, and evolution remain poorly understood. Results We report the isolation of the second member of Atribacterota, Thermatribacter velox gen. nov., sp. nov., within a new family Thermatribacteraceae fam. nov., and the short-term laboratory cultivation of a member of the JS1 lineage, Phoenicimicrobium oleiphilum HX-OS.bin.34TS, both from a terrestrial oil reservoir. Physiological and metatranscriptomics analyses showed that Thermatribacter velox B11T and Phoenicimicrobium oleiphilum HX-OS.bin.34TS ferment sugars and n-alkanes, respectively, producing H2, CO2, and acetate as common products. Comparative genomics showed that all members of the Atribacterota lack a complete Wood-Ljungdahl Pathway (WLP), but that the Reductive Glycine Pathway (RGP) is widespread, indicating that the RGP, rather than WLP, is a central hub in Atribacterota metabolism. Ancestral character state reconstructions and phylogenetic analyses showed that key genes encoding the RGP (fdhA, fhs, folD, glyA, gcvT, gcvPAB, pdhD) and other central functions were gained independently in the two classes, Atribacteria (OP9) and Phoenicimicrobiia (JS1), after which they were inherited vertically; these genes included fumarate-adding enzymes (faeA; Phoenicimicrobiia only), the CODH/ACS complex (acsABCDE), and diverse hydrogenases (NiFe group 3b, 4b and FeFe group A3, C). Finally, we present genome-resolved community metabolic models showing the central roles of Atribacteria (OP9) and Phoenicimicrobiia (JS1) in acetate- and hydrocarbon-rich environments. Conclusion Our findings expand the knowledge of the diversity, physiology, ecology, and evolution of the phylum Atribacterota. This study is a starting point for promoting more incisive studies of their syntrophic biology and may guide the rational design of strategies to cultivate them in the laboratory.

Genome analysis is one of the main criteria for description of new taxa. Availability of genome sequences for all the actinobacteria with a valid nomenclature will, however, require another decade’s works of sequencing. This paper describes the rearrangement of the higher taxonomic ranks of the members of the phylum ‘ Actinobacteria ’, using the phylogeny of 16S rRNA gene sequences and supported by the phylogeny of the available genome sequences. Based on the refined phylogeny of the 16S rRNA gene sequences, we could arrange all the members of the 425 genera of the phylum ‘ Actinobacteria ’ with validly published names currently in use into six classes, 46 orders and 79 families, including 16 new orders and 10 new families. The order Micrococcales Prévot 1940 (Approved Lists 1980) emend. Nouioui et al. 2018 is now split into 11 monophyletic orders: the emended order Micrococcales and ten proposed new orders Aquipuribacterales , Beutenbergiales , Bogoriellales , Brevibacteriales , Cellulomonadales , Demequinales , Dermabacterales , Dermatophilales , Microbacteriales and Ruaniales . Further, the class ‘ Actinobacteria ’ Stackebrandt et al. 1997 emend. Nouioui et al. 2018 was described without any nomenclature type, and therefore the name ‘ Actinobacteria ’ is deemed illegitimate. In accordance to Rule 8 of the International Code of Nomenclature of Prokaryotes, Parker et al. 2019, we proposed the name Actinomycetia which is formed by using the stem of the name Actinomycetales Buchanan 1917 (Approved Lists 1980) emend. Zhi et al. 2009, to replace the name ‘ Actinobacteria ’. The nomenclature type of the proposed new class Actinomycetia is the order Actinomycetales Buchanan 1917 (Approved Lists 1980) emend. Zhi et al. 2009.