1. Evolution of BchC: an enzyme required for the synthesis of bacteriochlorophyll a — Introduction

I published in 2016 a little paper in PLoS ONE about the evolution of BchF (Cardona 2016), an enzyme in the pathway to make bacteriochlorophyll a. In this project, I will present data and analysis on the evolution of another enzyme required to make bacteriochlorophyll a, that is: BchC. As far as I know, there are no evolutionary studies on this enzyme, so I plan to update my progress in here. Not sure where this will lead, but let’s keep an open mind, and lets keep it informal. I welcome your feedback and your participation!

I would say that there are 2 types of anoxygenic phototrophs described so far. Those which use bacteriochlorophyll a as ‘primary’ pigment and those which use bacteriochlorophyll g.

Those with bacteriochlorophyll a are:

• Proteobacteria
• Gemmatimonadetes
• Acidobacteria
• Chloroflexi
• Chlorobi

Those with bacteriochlorophyll g are:

• Heliobacteira

Cyanobacteria, which are the only bacteria capable of oxygenic photosynthesis do not use any form of bacteriochlorophyll. They use chlorophyll a as the primary pigment, and other chlorophylls derived from it, like chlorophyll d and f.

So this is the thing:

To make bacteriochlorophyll you first need to make the chlorophyll a precursor, chlorophyllide a. Chlorophyllide a is produced from protochlorophyllide, and the reaction is catalysed by the ChlLNB enzyme, the one homologous to nitrogenases. If you attach a tale directly to chlorophyllide a, then it becomes chlorophyll a, which is used by Cyanobacteria and photosynthetic eukaryotes. However, Acidobacteria, Chlorobi, and Heliobacteria also make chlorophyll a in addition to their primary bacteriochlorophylls and use it in their homodimeric Type I reaction centres.

To make bacteriochlorophyll g, you need the enzyme BchXYZ, which is homologous to ChlLNB and the nitrogenases as well. That takes chlorophyllide a and makes bacteriochlorophyllide. If you put a tail to it, without any further modifications, it becomes bacteriochlorophyll g (Tsukatani et al. 2013).

To make bacteriochlorophyll a, you need BchXYZ, and two additional enzymes not found in Cyanobacteria nor Heliobacteria, these are BchF and BchC. After these two extra steps, you add a tail and then you have—finally—bacteriochlorophyll a.

It seems to me that some of the earliest phototrophs likely made both chlorophyll a and bacteriochlorophyll g. Or something like those, using the ancestral enzymes to LNB and XYZ, or the early versions of these. And only at a later stage, bacteriochlorophyll a was invented by adding BchF and BchC. And, I think, the addition of BchF and BchC happened in an ancestral bacterium predating the divergence of Chlorobi, Chloroflexi, Proteobacteria, and Acidobacteria... but already after the branching of some early groups of phototrophic Firmicutes, of which only Heliobacteria survives (or has been discovered).

And I also think the reason why bacteriochlorophyll a was invented is because bacteriochlorophyll g reacts with oxygen and bleaches really quickly.

I like an scheme presented in 1987 by Olson and Pierson, see the attached figure (Olson and Pierson 1987). I think they got pretty close! I have made some adjustments, which reflects more what I think… not exactly, but it will do for now.

And scheme by Olson and Pierson 1987 on the evolution of reaction centres and chlorophylls, with my modifications!

So, I suspect that bacteriochlorophyll a evolved at a relatively late stage, already when there was enough oxygen around to cause some damage. My hypothesis is that it evolved to stabilize the pigment in the presence of oxygen. In my PLoS ONE paper I argued that the phylogeny of BchF, if compared to that of Type I and Type II reaction centre proteins, suggests that when BchF appeared, both reaction centres had already diverged.

An interesting question is, when did bacteriochlorophyll a appear relative to bacteriochlorophyll g? I will attempt to measure this at some point.

Now, the evolution of BchC could also hold some interesting clues on the origin of bacteriochlorophyll a-based photosynthesis. And that is why I will present here some data, as I produce it, on the evolution of BchC. I already have some phylogenetic trees...

References

Cardona, T. (2016). "Origin of Bacteriochlorophyll a and the Early Diversification of Photosynthesis." PLoS One 11(3): e0151250.

Olson, J. M. and B. K. Pierson (1987). "Origin and Evolution of Photosynthetic Reaction Centers." Origins of Life and Evolution of the Biosphere 17(3-4): 419-430.

Tsukatani, Y., H. Yamamoto, T. Mizoguchi, Y. Fujita and H. Tamiaki (2013). "Completion of biosynthetic pathways for bacteriochlorophyll g in Heliobacterium modesticaldum: The C8-ethylidene group formation." Biochimica Et Biophysica Acta-Bioenergetics 1827(10): 1200-1204.