Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial Phylum<i>Candidatus</i>Palusbacterota (WPS-2)

Ward, Lewis M.; Cardona, Tanai; Holland‐Moritz, Hannah

doi:10.1101/534180

Cited by 8 publications

(6 citation statements)

References 85 publications

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“…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.…”

Section: Resultsmentioning

confidence: 98%

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

et al. 2019

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There is a long and rich history of literature on phototrophs in terrestrial geothermal springs. These studies have revealed sulfide, pH, and temperature are the main constraints on phototrophy. However, the taxonomic and physiological diversity of anoxygenic phototrophs suggests that, within these constraints, specific geochemical parameters determine the distribution and activity of individual anoxygenic phototrophic taxa. Here, we report the recovery of sequences affiliated with characterized anoxygenic phototrophs in sites that range in pH from 2 to 9 and in temperature from 31°C to 71°C. Transcript abundance indicates anoxygenic phototrophs are active across this temperature and pH range. Our data suggest sulfide is not a key determinant of anoxygenic phototrophic taxa and underscore a role for photoheterotrophy in terrestrial geothermal ecosystems. These data provide the framework for high-resolution sequencing and in situ activity approaches to characterize the physiology of specific anoxygenic phototrophic taxa across a broad range of temperatures and pH.

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Section: Resultsmentioning

confidence: 98%

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

et al. 2019

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“…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.…”

Section: Taxon-rich Multi-rp Trees Are Reasonably Accurate Within Domainsmentioning

confidence: 99%

“…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.…”

Section: Eubacteria Were Ancestrally Photosyntheticmentioning

confidence: 99%

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

Cavalier‐Smith

Chao

2020

Protoplasma

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Palaeontologically, eubacteria are > 3× older than neomura (eukaryotes, archaebacteria). Cell biology contrasts ancestral eubacterial murein peptidoglycan walls and derived neomuran N-linked glycoprotein coats/walls. Misinterpreting long stems connecting clade neomura to eubacteria on ribosomal sequence trees (plus misinterpreted protein paralogue trees) obscured this historical pattern. Universal multiprotein ribosomal protein (RP) trees, more accurate than rRNA trees, are taxonomically undersampled. To reduce contradictions with genically richer eukaryote trees and improve eubacterial phylogeny, we constructed site-heterogeneous and maximum-likelihood universal three-domain, two-domain, and single-domain trees for 143 eukaryotes (branching now congruent with 187-protein trees), 60 archaebacteria, and 151 taxonomically representative eubacteria, using 51 and 26 RPs. Site-heterogeneous trees greatly improve eubacterial phylogeny and higher classification, e.g. showing gracilicute monophyly, that many ‘rDNA-phyla’ belong in Proteobacteria, and reveal robust new phyla Synthermota and Aquithermota. Monoderm Posibacteria and Mollicutes (two separate wall losses) are both polyphyletic: multiple outer membrane losses in Endobacteria occurred separately from Actinobacteria; neither phylum is related to Chloroflexi, the most divergent prokaryotes, which originated photosynthesis (new model proposed). RP trees support an eozoan root for eukaryotes and are consistent with archaebacteria being their sisters and rooted between Filarchaeota (=Proteoarchaeota, including ‘Asgardia’) and Euryarchaeota sensu-lato (including ultrasimplified ‘DPANN’ whose long branches often distort trees). Two-domain trees group eukaryotes within Planctobacteria, and archaebacteria with Planctobacteria/Sphingobacteria. Integrated molecular/palaeontological evidence favours negibacterial ancestors for neomura and all life. Unique presence of key pre-neomuran characters favours Planctobacteria only as ancestral to neomura, which apparently arose by coevolutionary repercussions (explained here in detail, including RP replacement) of simultaneous outer membrane and murein loss. Planctobacterial C-1 methanotrophic enzymes are likely ancestral to archaebacterial methanogenesis and β-propeller-α-solenoid proteins to eukaryotic vesicle coats, nuclear-pore-complexes, and intraciliary transport. Planctobacterial chaperone-independent 4/5-protofilament microtubules and MamK actin-ancestors prepared for eukaryote intracellular motility, mitosis, cytokinesis, and phagocytosis. We refute numerous wrong ideas about the universal tree.

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

Section: Author’s Notementioning

confidence: 99%

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

2019

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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 proposed in the uncultured bacterial WPS-2 phylum (recently proposed as Candidatus Eremiobacterota) 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 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 Baltobacterales for the order-level aerobic WPS-2 clade which contains phototrophic lineages, from the Greek for "bog" or "swamp," in reference to the typical habitat of phototrophic members of this clade.

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

Cited by 8 publications

References 85 publications

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

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

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

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

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