The changing landscape of microbial biodiversity exploration and its implications for systematics

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A vast diversity of Bacteria and Archaea exists in nature that has evaded axenic culture. Advancements in single-cell genomics, metagenomics, and molecular microbial ecology approaches provide ever-improving insight into the biology of this so-called “microbial dark matter”; however, due to the International Code of Nomenclature of Prokaryotes, yet-uncultivated microorganisms are not accommodated in formal taxonomy regardless of the quantity or quality of data. Meanwhile, efforts to calibrate the existing taxonomy with phylogenetic anchors and genomic data are increasingly robust. The current climate provides an exciting opportunity to leverage rapidly expanding single-cell genomics and metagenomics datasets to improve the taxonomy of Bacteria and Archaea. However, this opportunity must be weighted carefully in light of the strengths and limitations of these approaches. We propose to expand the definition of the Candidatus taxonomy to include taxa, from the phylum level to the species level, that are described genomically, particularly when genomic work is coupled with advanced molecular ecology approaches to probe metabolic functions in situ. This system would preserve the rigor and value of traditional microbial systematics while enabling growth of a provisional taxonomic structure to facilitate communication about “dark” lineages on the tree of life.