Fig 1.
Unrooted phylogeny of bacteria built with concatenated ribosomal protein sequences, following [22] with additional data from newly described phototrophs in the phylum Eremiobacterota (here labeled by their alternate name WPS2) [21,23] and the Chloroflexi class Anaerolineae [19].
Occurrences of reaction center-based phototrophy within a phylum indicated by shading of the entire phylum, color coded by reaction center type (RC1 for Type 1 anoxygenic reactions centers, RC2 for Type 2 anoxygenic reaction centers, PSI for photosystem 1, PSII for photosystem 2). For clarity, the entire phylum is highlighted even when phototrophy is restricted to only some members (e.g. the phototrophic Heliobacteria within the much broader, predominantly nonphototrophic, Firmicutes phylum).
Table 1.
Traits of extant phototroph lineages.
Fig 2.
Tanglegrams demonstrating phylogenetic incongruities between separate components of phototrophy pathways, including reaction centers, backbone (bacterio)chlorophyll synthesis, and the BchXYZ complex involved in bacteriochlorophyll synthesis; red lines indicate phyla with distinct branching order in phylogenies on the left and right, likely reflecting independent histories of horizontal gene transfer.
Taxon abbreviations: Cf, Chloroflexi; Cb, Chlorobi; W, WPS2/Eremiobacterota; Ca, Chloracidobacteria; H, Heliobacteria; P, Proteobacteria (including Gemmatimonadetes); Cy, Cyanobacteria.
Fig 3.
Cartoon overlayed phylogenies to demonstrate hypothesized history of HGT and ghost lineage.
Underlying topology derived from backbone (bacterio)chlorophyll synthesis genes (BchH/D/I/M) (black). BchLNB and BchXYZ are derived from a common ancestor in stem group phototrophs. BchLNB (green) was inherited together with BchHDIM into extant phototrophs; BchXYZ (red) diverged in the ghost lineage before being introduced into extant anoxygenic phototrophs via HGT (a first HGT event introduced it into the stem of the proteobacterial lineage; a second HGT event introduced it into the stem of the WPS2/Chlorobi/Chloroflexi lineage; subsequent HGT introduced it into the Chloracidobacteria and Heliobacteria lineages). Type 1 reaction centers (RC1 and PSI) and Type 2 reaction centers (RC2 and PSII) diverged in stem lineage phototrophs. Type 1 reaction centers (peach) were vertically inherited into extant phototrophic lineages. Type 2 reaction centers (blue) diverged in the same ghost lineage as BchXYZ, and were introduced into extant clades via HGT (first into stem group Cyanobacteria, leading to PSII, then into stem group Proteobacteria and the stem lineage of WPS2, Chloroflexi, and Chlorobi). The most parsimonious history consistent with the data involves a secondary replacement of RC2 with RC1 in Chlorobi. Alternative evolutionary histories are similarly parsimonious, but all involve many events of HGT of individual phototrophy components and most involve secondary loss and replacement in some lineages. The inclusion of one or more ghost lineages improves parsimony and provides a good explanation for long branches between RC1/RC2 and BchLNB/BchXYZ homolog pairs. A summary of hypothesized HGT events is presented in Table 2.
Table 2.
Hypothesized HGT events of phototrophy modules.
Fig 4.
Cartoon timeline of phototroph evolution as hypothesized here.
The “ancestral” phototroph was anoxygenic and utilized chlorophyll pigments, adapted to high light. At least two lineages of phototrophs diverged during Archean time, giving rise to the ancestors of Type 1 Reaction Centers and the BchLNB complex, and the Type 2 Reaction Centers and the BchXYZ complex. Eventually, HGT of a Type 2 RC into an RC1 and BchLNB-containing proto-cyanobacterium enabled the evolution of oxygenic photosynthesis, still using chlorophyll pigments. As oxygenated surface waters and competition with Cyanobacteria forced anoxygenic phototrophs into lower light regions of the water column or microbial mats (where oxygen is lower and electron donors are more abundant), they underwent adaptation to lower quality light. This included the HGT of BchXYZ complexes into BchLNB-containing lineages, allowing the innovation of bacteriochlorophyll pigments, probably first with bchl a. Eventually, anoxygenic phototrophs diversified in terms of organisms (including extant groups), pigments (bchl c-g), and reaction centers (further HGT of RC2). Oxygenic phototrophy diversified via eukaryotic endosymbiosis (primary and higher order) and colonization of land by plants. While the relative timing of these events can be inferred from comparative biology, absolute timing of many of these events is only poorly constrained if at all, based on the sparse microfossil and biomarker record of early phototrophic microbes and molecular clock estimates for the antiquity of crown group clades.