The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria
Sara C Di Rienzi,
Itai Sharon,
Kelly C Wrighton,
Omry Koren,
Laura A Hug,
Brian C Thomas,
Julia K Goodrich,
Jordana T Bell,
Timothy D Spector,
Jillian F Banfield,
Ruth E Ley
Affiliations
Sara C Di Rienzi
Department of Microbiology, Cornell University, Ithaca, United States
Itai Sharon
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, United States
Kelly C Wrighton
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, United States
Omry Koren
Department of Microbiology, Cornell University, Ithaca, United States
Laura A Hug
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, United States
Brian C Thomas
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, United States
Julia K Goodrich
Department of Microbiology, Cornell University, Ithaca, United States
Jordana T Bell
Department of Twin Research and Genetic Epidemiology, King’s College London, London, United Kingdom
Timothy D Spector
Department of Twin Research and Genetic Epidemiology, King’s College London, London, United Kingdom
Jillian F Banfield
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, United States; Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, United States
Ruth E Ley
Department of Microbiology, Cornell University, Ithaca, United States
Cyanobacteria were responsible for the oxygenation of the ancient atmosphere; however, the evolution of this phylum is enigmatic, as relatives have not been characterized. Here we use whole genome reconstruction of human fecal and subsurface aquifer metagenomic samples to obtain complete genomes for members of a new candidate phylum sibling to Cyanobacteria, for which we propose the designation ‘Melainabacteria’. Metabolic analysis suggests that the ancestors to both lineages were non-photosynthetic, anaerobic, motile, and obligately fermentative. Cyanobacterial light sensing may have been facilitated by regulators present in the ancestor of these lineages. The subsurface organism has the capacity for nitrogen fixation using a nitrogenase distinct from that in Cyanobacteria, suggesting nitrogen fixation evolved separately in the two lineages. We hypothesize that Cyanobacteria split from Melainabacteria prior or due to the acquisition of oxygenic photosynthesis. Melainabacteria remained in anoxic zones and differentiated by niche adaptation, including for symbiosis in the mammalian gut.