Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial PhylumCandidatusPalusbacterota (WPS-2)

Abstract

Genome-resolved environmental metagenomic sequencing has uncovered substantial previously unrecognized microbial diversity relevant for understanding the ecology and evolution of the biosphere, providing a more nuanced view of the distribution and ecological significance of traits including phototrophy across diverse niches. Recently, the capacity for bacteriochlorophyll-based anoxygenic photosynthesis has been found in the uncultured bacterial WPS-2 clade that are in close association with boreal moss. Here, we use phylogenomic analysis to investigate the diversity and evolution of phototrophic WPS-2. We demonstrate that phototrophic WPS-2 show significant genetic and metabolic divergence from other phototrophic and non-phototrophic lineages. The genomes of these organisms encode a completely new family of anoxygenic Type II photochemical reaction centers and other phototrophy-related proteins that are both phylogenetically and structurally distinct from those found in previously described phototrophs. We propose the name Candidatus Palusbacterota for the phylum-level aerobic WPS-2 clade which contains phototrophic lineages, from the Latin for "bog bacteria", distinguishing it from the anaerobic, non-phototrophic sister phylum Candidatus Eremiobacterota for "desert bacteria", typically found in dry environments.

Anoxygenic Phototrophs Span Geochemical Gradients and Diverse Morphologies in Terrestrial Geothermal Springs

“…We also observed small numbers of 16S rRNA gene sequences assigned to the proposed phylum “ Candidatu s Palusbacterota” (formerly phylum WPS-2) (Fig. S4) (71). In metagenomic data, members of “ Candidatu s Palusbacterota” encode type II reaction centers, and members of this proposed phylum are thought to inhabit acidic, aerobic environments.…”

Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria)

“…Their branching order is otherwise very stable on site-heterogeneous trees restricted to Eubacteria, but adding one or both highly divergent neomuran groups on multidomain trees makes branching order less stable, there being a strong tendency for the major thermophilic phyla (Aquithermota, Synthermota) to group together or become partially intermixed with Hadobacteria/Fusobacteria; these changes are likely artefacts. Phyla with some photosynthetic members are in green; the different types of photosynthetic reaction centres (RC and characteristic deletions) and presence of FMO, chlorins, phycobilisomes (PB) and chlorosomes (cs) are mapped onto the tree; it is unknown if uncultured Candidatus Palusbacteriales ('Eremiobacteria': Ward et al 2019) has chlorosomes-as not in our analyses, its likely position in Armatimonadetes (dashed line) is only weakly established; its discovery increases the likelihood that ancestral eubacteria (i.e. LUCA) had RCII.…”

“…The great antiquity of photosynthesis by L/M reaction centres is reinforced by an eighth lineage known only from environmental DNA sequencing ('Eremiobacterota' = WPS-2 'candidate phylum': Ji et al 2017) which is sister to Armatimonadetes on 38-protein trees by FastTree (less accurate than ML) apparently having distinctive L/M reaction centres and RuBisCo in four sublineages from boreal mosses (Holland-Moritz et al 2018;Ward et al 2019). L and M proteins are most closely related to those of Chloroflexi but so distant that we cannot infer LGT from one to the other, making it probable that the common ancestor of Chloroflexi and WPS-2 was photosynthetic and both lineages multiply lost photosynthesis.…”

Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial Phylum Candidatus Eremiobacterota (WPS-2)

“…A version of this manuscript prior to peer review has been released as a preprint by Ward et al (2019a).…”