Evidence for the presence of key chlorophyll-biosynthesis-related proteins in the genus Rubrobacter (Phylum Actinobacteria) and its implications for the evolution and origin of photosynthesis

Abstract

Homologs showing high degree of sequence similarity to the three subunits of the protochlorophyllide oxidoreductase enzyme complex (viz. BchL, BchN, and BchB), which carries out a central role in chlorophyll-bacteriochlorophyll (Bchl) biosynthesis, are uniquely found in photosynthetic organisms. The results of BLAST searches and homology modeling presented here show that proteins exhibiting a high degree of sequence and structural similarity to the BchB and BchN proteins are also present in organisms from the high G+C Gram-positive phylum of Actinobacteria, specifically in members of the genus Rubrobacter (R. x ylanophilus and R. r adiotolerans). The results presented exclude the possibility that the observed BLAST hits are for subunits of the nitrogenase complex or the chlorin reductase complex. The branching in phylogenetic trees and the sequence characteristics of the Rubrobacter BchB/BchN homologs indicate that these homologs are distinct from those found in other photosynthetic bacteria and that they may represent ancestral forms of the BchB/BchN proteins. Although a homolog showing high degree of sequence similarity to the BchL protein was not detected in Rubrobacter, another protein, belonging to the ParA/Soj/MinD family, present in these bacteria, exhibits high degree of structural similarity to the BchL. In addition to the BchB/BchN homologs, Rubrobacter species also contain homologs showing high degree of sequence similarity to different subunits of magnesium chelatase (BchD, BchH, and BchI) as well as proteins showing significant similarity to the BchP and BchG proteins. Interestingly, no homologs corresponding to the BchX, BchY, and BchZ proteins were detected in the Rubrobacter species. These results provide the first suggestive evidence that some form of photosynthesis either exists or was anciently present within the phylum Actinobacteria (high G+C Gram-positive) in members of the genus Rubrobacter. The significance of these results concerning the origin of the Bchl-based photosynthesis is also discussed.

A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments

“…We found a wide variety of carbohydrate-active enzymes in these MAGs, such as cellulases (GH1 family) in addition to genes for glycolysis and TCA cycle and a chlorophyll/bacteriochlorophyll a/b synthase ( bchG gene). The latter was also found in other Actinobacteria from the genus Rubrobacter [ 39 ]. No evidence was found for nitrile-degrading potential.…”

Origin of Bacteriochlorophyll a and the Early Diversification of Photosynthesis

“…It is overall very similar to other phylogenomic trees, and the relationship of phyla containing phototrophic strains is virtually identical to those presented before, see for example Jun et al [ 20 ], who implemented an alignment free approach. The phyla of bacteria highlighted in color represent those with photochemical reaction centers, with the exception of Actinobacteria that only recently was suggested to have been ancestrally phototrophic [ 2 ]. The colored transparent lines that are overlaid on top of the phylogenomic tree represent the evolution of the selected proteins.…”

“…Because of these adaptations to land habitats, Battistuzzi et al called this supergroup Terrabacteria; and the supergroup that contained Proteobacteria, Acidobacteria, Chlorobi, and closely related non-phototrophic groups, Hydrobacteria [ 19 ]. Taking into account that both Chloroflexi and Cyanobacteria are capable of photosynthesis, and adding to this the possibility that Actinobacteria was ancestrally capable of photosynthesis [ 2 ], it starts to look increasingly likely that this supergroup was also ancestrally phototrophic. There is a common unifying characteristic between these two supergroups: Type I and Type II reaction centers are found in both of them.…”

“…These are Cyanobacteria, Proteobacteria, Firmicutes, Chloroflexi, Chlorobi, Acidobacteria, and Gemmatimonadetes [ 1 ]. In addition, a recent study suggested that a few strains in the phylum Actionabecteria may retain what appears to be a vestigial chlorophyll synthesis pathway [ 2 ]. From these groups, only Proteobacteria, Chloroflexi, Chlorobi, Acidobacteria, and Gemmatimonadetes are capable of synthetizing bacteriochlorophyll a .…”

Reconstructing the Origin of Oxygenic Photosynthesis: Do Assembly and Photoactivation Recapitulate Evolution?

“…Within Bacteria, there are currently seven phyla known to have strains with reaction centers, these are: Cyanobacteria, Chloroflexi, Firmicutes, Chlorobi, Proteobacteria, and those recently found in Acidobacteria (Bryant et al, 2007 ; Tsukatani et al, 2012 ) and Gemmatimonadetes (Zeng et al, 2014 , 2015 ). Just a while ago, it was suggested that the phylum Actinobacteria might have been ancestrally capable of photosynthesis (Gupta and Khadka, 2016 ), as some strains in this phylum seem to have a vestigial chlorophyll synthesis pathway. Although a consensus on the type of bacteria in which photochemical reaction centers originated is lacking, it is understood that both Type I and Type II reaction centers have a common origin.…”