Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Abstract

Various lines of evidence from both comparative biology and the geologic record make it clear that the biochemical machinery for anoxygenic photosynthesis was present on early Earth and provided the evolutionary stock from which oxygenic photosynthesis evolved ca. 2.3 billion years ago. However, the taxonomic identity of these early anoxygenic phototrophs is uncertain, including whether or not they remain extant. Several phototrophic bacterial clades are thought to have evolved before oxygenic photosynthesis emerged, including the Chloroflexi, a phylum common across a wide range of modern environments. Although Chloroflexi have traditionally been thought to be an ancient phototrophic lineage, genomics has revealed a much greater metabolic diversity than previously appreciated. Here, using a combination of comparative genomics and molecular clock analyses, we show that phototrophic members of the Chloroflexi phylum are not particularly ancient, having evolved well after the rise of oxygen (ca. 867 million years ago), and thus cannot be progenitors of oxygenic photosynthesis. Similarly, results show that the carbon fixation pathway that defines this clade-the 3-hydroxypropionate bicycleevolved late in Earth history as a result of a series of horizontal gene transfer events, explaining the lack of geological evidence for this pathway based on the carbon isotope record. These results demonstrate the role of horizontal gene transfer in the recent metabolic innovations expressed within this phylum, including its importance in the development of a novel carbon fixation pathway.carbon fixation | phototrophy | molecular clock | comparative genomics F rom both biological and geological data, it is widely thought that anoxygenic photosynthesis preceded the development of oxygenic photosynthesis and the rise of atmospheric oxygen (1). Although it has been largely accepted that oxygenic photosynthesis evolved in ancient Cyanobacterial lineages (2), very little is known about the nature and evolutionary history of anoxygenic phototrophy, with most of our understanding stemming from assumptions and hypotheses based on the few extant bacterial taxa that host this metabolism. Given the significance of the accumulation of oxygen ca. ∼2.3 billion years ago, it is of no surprise that the majority of efforts have focused on studying oxygenic photosynthesis. However, this has resulted in a paucity of studies critically examining basic and core questions on the origins of anoxygenic photosynthesis, such as what bacterial lineage developed this metabolism and when did it evolve? These questions are essential to our first-order knowledge of how early microbial metabolisms may have shaped the geochemical cycles of our planet.Although chlorophyll-based photosynthesis can be found in seven known bacterial phyla (i.e

Early Archean origin of Photosystem II

“…That anoxygenic phototrophs are displaying higher rates of evolution than Cyanobacteria is supported by other independent molecular clock studies (Magnabosco, Moore, Wolfe, & Fournier, ; Shih, Ward, & Fischer, ). For example, the level of sequence identity between L in Roseiflexus castenholzii and L in Chloroflexus sp.…”

“…If the estimated age reported by Shih, Ward et al. () is correct, that would make the rate of evolution of L in the Chloroflexi about 5.5 times faster than D1 or D2 (1% loss for every ~100 Ma assuming Gloeobacter branched out 2.0 Ga ago). Magnabosco et al.…”

“…Shih, Ward et al. () calculated that the MRCA of phototrophic Chloroflexi occurred about 1.0 Ga ago. That date would imply that the L in Roseiflexus and Chloroflexus lost 55% sequence identity since their most recent common ancestor about 1.0 Ga ago (1% loss for every ~18 Ma).…”

“…Our results are consistent with the emerging view that most, if not all, identified groups of phototrophs started to diversify long after the origin of photosynthesis. Recent molecular clock analysis aimed at dating the MRCA of various groups of phototrophs have concluded that these appeared at around the GOE or after the GOE (Cardona, ; Magnabosco et al., ; Shih, Hemp et al., ; Shih, Ward et al., ). Our results support this view, yet at the same time they highlight the great antiquity of photosynthesis by showing that some of the early duplications of the core reaction center proteins likely predate the MRCA of each of the known groups of phototrophs by a large span of time.…”

Phototrophic Methane Oxidation in a Member of the Chloroflexi Phylum

“…The coupling of methanotrophy or propanotrophy to phototrophy would be enabled by the modular nature of high-potential electron transfer pathways (Ward et al 2018a, Shih et al 2017). Electrons derived from oxidation of single-carbon compounds or short alkanes can be fed into the phototrophic reaction center to drive cyclic electron flow for energy conservation and subsequently used for carbon fixation (Figure 4).…”