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

Lewis M Ward,Hannah Holland-Moritz,Tanai Cardona

doi:10.3389/fmicb.2019.01658

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.

Highlights

The vast majority of primary productivity on Earth is fueled by photosynthesis, both today (Raven, 2009) and through most of the history of life (Kharecha et al, 2005; Canfield et al, 2006; Ward et al, 2019b), making the organisms and proteins responsible for driving photosynthesis into critical bases for the carbon cycle
Unlike oxygenic photosynthesis which requires the work of Type I and Type II photochemical reaction centers linked in series for water oxidation, anoxygenic phototrophs use exclusively either Type I or Type II reaction centers
These have traditionally been subdivided into two types, the L and M found in the reaction centers of phototrophic Proteobacteria (PbRC) and the L and M found in those of the phototrophic Chloroflexi (CfRC), with each set making deep-branching monophyletic clades (Beanland, 1990; Cardona, 2015)

Summary

Introduction

The vast majority of primary productivity on Earth is fueled by photosynthesis, both today (Raven, 2009) and through most of the history of life (Kharecha et al, 2005; Canfield et al, 2006; Ward et al, 2019b), making the organisms and proteins responsible for driving photosynthesis into critical bases for the carbon cycle. There are only five phyla of bacteria known to have phototrophic representatives that use anoxygenic Type II reaction centers: Proteobacteria, Chloroflexi, and Gemmatimonadetes (Zeng et al, 2014), recent evidence for potential phototrophy in one isolate in the Bacteroidetes (Tahon and Willems, 2017), and the newly discovered WPS-2 (Holland-Moritz et al, 2018; Figure 1). The photochemical pigments of anoxygenic Type II reaction centers are bound by two homologous subunits known as L (PufL) and M (PufM) These have traditionally been subdivided into two types, the L and M found in the reaction centers of phototrophic Proteobacteria (PbRC) and the L and M found in those of the phototrophic Chloroflexi (CfRC), with each set making deep-branching monophyletic clades (Beanland, 1990; Cardona, 2015). Proteobacterial pufLM genes may have been detected in strains of the genus Alkalibacterium of the phylum Firmicutes from perennial springs of the high arctic (Perreault et al, 2008)

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Conclusion