Dataset Information

Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial Phylum Candidatus Eremiobacterota (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 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.

SUBMITTER: Ward LM

PROVIDER: S-EPMC6664022 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Publications

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

Ward Lewis M LM Cardona Tanai T Holland-Moritz Hannah H

Frontiers in microbiology 20190723

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 <i>Candidatus ...[more]

PMID: 31396180

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Project description:Acidophilic archaea of the archaeal Richmond Mine acidophilic nanoorganisms (ARMAN) group from the uncultured candidate phylum "Candidatus Micrarchaeota" have small genomes and cell sizes and are known to be metabolically dependent and physically associated with their Thermoplasmatales hosts. However, phylogenetically diverse "Ca Micrarchaeota" are widely distributed in various nonacidic environments, and it remains uncertain because of the lack of complete genomes whether they are also devoted to a partner-dependent lifestyle. Here, we obtained nine metagenome-assembled genomes of "Ca Micrarchaeota" from the sediments of a meromictic freshwater lake, including a complete, closed 1.2 Mbp genome of "Ca Micrarchaeota" Sv326, an archaeon phylogenetically distant from the ARMAN lineage. Genome analysis revealed that, contrary to ARMAN "Ca Micrarchaeota," the Sv326 archaeon has complete glycolytic pathways and ATP generation mechanisms in substrate phosphorylation reactions, the capacities to utilize some sugars and amino acids as substrates, and pathways for de novo nucleotide biosynthesis but lacked an aerobic respiratory chain. We suppose that Sv326 is a free-living scavenger rather than an obligate parasite/symbiont. Comparative analysis of "Ca Micrarchaeota" genomes representing different order-level divisions indicated that evolution of the "Ca Micrarchaeota" from a free-living "Candidatus Diapherotrites"-like ancestor involved losses of important metabolic pathways in different lineages and gains of specific functions in the course of adaptation to a partner-dependent lifestyle and specific environmental conditions. The ARMAN group represents the most pronounced case of genome reduction and gene loss, while the Sv326 lineage appeared to be rather close to the ancestral state of the "Ca Micrarchaeota" in terms of metabolic potential.IMPORTANCE The recently described superphylum DPANN includes several phyla of uncultivated archaea with small cell sizes, reduced genomes, and limited metabolic capabilities. One of these phyla, "Ca Micrarchaeota," comprises an enigmatic group of archaea found in acid mine drainage environments, the archaeal Richmond Mine acidophilic nanoorganisms (ARMAN) group. Analysis of their reduced genomes revealed the absence of key metabolic pathways consistent with their partner-associated lifestyle, and physical associations of ARMAN cells with their hosts were documented. However, "Ca Micrarchaeota" include several lineages besides the ARMAN group found in nonacidic environments, and none of them have been characterized. Here, we report a complete genome of "Ca Micrarchaeota" from a non-ARMAN lineage. Analysis of this genome revealed the presence of metabolic capacities lost in ARMAN genomes that could enable a free-living lifestyle. These results expand our understanding of genetic diversity, lifestyle, and evolution of "Ca Micrarchaeota."

Dataset Information

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

Publications

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

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