The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria

Abstract

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.DOI: http://dx.doi.org/10.7554/eLife.01102.001

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

“…We expanded the fermentative capacity of CP (for example, OD1, WWE3 and OP11) to include possible roles in cellulose and chitin degradation, as well as assigning roles in carbon degradation and hydrogen production to a member of a new phylum, sibling to Cyanobacteria (ACD20, Melainabacteria), Bacteroidales (ACD77) and Anaerolineae (ACD34) (Figure 4). Draft genomes for members of the Anaerolineae have been documented in unamended sediments from this same aquifer and complete genomes from the Melainabacteria lineage were recovered from the human intestinal tract (Di Rienzi et al, 2013). Conclusions from these studies are consistent with our proposed roles in carbon degradation, suggesting a conserved functionality across ecosystems may exist for some of the organisms identified here.…”

“…A recovered 16S rRNA gene places ACD64, a partial genome bin, in the TM6 lineage and ACD58, previously reported as a divergent OD1 in Wrighton et al (2012), is now recognized as a separate phylum level lineage, here named Berkelbacteria. For another near-complete genome, ACD20, we used a combination of core and 16S rRNA genes (o85% identity) assign the organism to a novel phylum called Melainabacteria, most closely related to the Cyanobacteria (Di Rienzi et al, 2013; Figure 1). Another near-complete genome, ACD47, lacks a 16S rRNA gene sequence but, based on our concatenated protein phylogenetic analyses, this genome represents a previously genomically unsampled phylum (Figure 1, Supplementary Figure S5e).…”

“…Consistent with this hypothesis, a significant fraction of organisms, including Melainabacteria (ACD20) and members of the OP11 and OD1, appear to be obligately fermentative, and express genes for in situ carbon degradation. This inference is based on the lack of a complete tricarboxylic acid cycle, electron transport chain components and terminal reductase/oxidases Di Rienzi et al, 2013).…”

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

“…Lau94 and Lau96), Cyanobacteria (Lau27), Melainabacteria (Lau2), Candidate Division TM7 (Saccharibacteria) (Lau1), Chloroflexi (Lau3 and Lau12), Marine Group A (Lau47, Lau103 and Lau104), Nitrospinae (Lau17), Nitrospirae (Lau44), Poribacteria (Lau21 and Lau377), Verrucomicrobia (Lau158, Lau184, Lau190 and Lau191), Acidobacteria (Lau40), Epsilonproteobacteria (Lau15, Lau129 and Lau229) and Gemmatimonadetes (Lau45) (Teske et al, 2002;Walsh et al, 2009;Swan et al, 2011;Yamamoto and Takai, 2011;Flores et al, 2012;Sylvan et al, 2012;Wright et al, 2012;Allers et al, 2013;Di Rienzi et al, 2013;Sylvan et al, 2013). Searches for eukaryotic SSU rRNA genes revealed the presence of novel populations of Archaeplastida, DH147-EKD23, Alveolata (Ciliophora, Dinoflagellata, OLI11255 and Protalveolata), Rhizaria and Opisthokonta (Fungi and Metazoa).…”

Core-satellite populations and seasonality of water meter biofilms in a metropolitan drinking water distribution system

“…The coresuspended community covers similar divisions, and also includes sequences related to the Candidatus phylum Melainabacteria that were genomically predicted as non-photosynthetic bacteria (Di Rienzi et al, 2013). The suspended community also harbored 'Candidatus Omnitrophica'-related sequences at low abundance.…”