Searching for new Type I reaction centre proteins in metagenomes

Testing my new-found metagenome-searching skills I decided to look for Type I reaction centre core subunits from Heliobacteria. This is because there are less than a handful of PshA sequences from this fascinating group of organisms, and only one complete and published sequenced genome.

Judging from the massive phylogenetic distance between the PshA core subunit of the reaction centre from Heliobacteria and the next closest relative (the PscA from Chlorobi/Acidobacteria), one must assume that a significant biodiversity should have existed spanning this distance, even if one or the other obtained phototrophy via horizontal gene transfer.

I limited my search to about 2000 metagenomes. I narrowed down my selection to those using in the metagenome title: “microbial dark matter”. I am not sure however if all of these belong to a singular project or if these have come from different/independent labs or projects.

I have always wondered however, if in these humongous datasets there are any novel phototrophs still unknown to science.

I used the PshA sequence from Heliobacterium modesticaldum as query.

The BLAST did not retrieve new sequence from Heliobacteria nor Acidobacteria, but did retrieve quite a few sequences from phototrophic Chlorobi and Cyanobacteria, see the attached figures. No sequences outside the known phyla of phototrophs were found, which is kind of sad. I had great expectations.

PscA from phototrophic Chlorobi

255 complete or almost complete sequences were obtained, which I then used to build a Maximum Likelihood tree. I did not have a look at fragmented sequences.

There was one almost complete sequence of a PsaA subunit from a new strain close to Gloeobacter.

It had 82% sequence identity to the PsaA of G. violaceus and G. kilaueensis. In comparison, the PsaA of these last two share 88% sequence identity. As another point of comparison, the level of sequence identity for PsaA between a red algae, C. merolae, and A. thaliana is 82%.

PsaA, the early branches. ML tree. In bold the metagenome sequnces

At this level of sequence divergence, it should be a new genus/species. I name this strain Protogloeobacter cardonensis. Kidding.

The metagenome where this particular sequence was found is the following:

Hot spring sediment bacterial and archeal communities from British Columbia, Canada, to study Microbial Dark Matter (Phase II) - Larsen N4 metaG (Released on 2016-05-27)

There were also quite a few sequences from the early-branching hot spring Synechococcus type. In addition, a PsaA/PsaB pair for another Gloeomargarita strain and a PsaA/PsaB pair of isoforms of the far-red light acclimation response from a form of Fischerella.

If you want the sequences or would like to see the full tree, let me know.

The atypical D1 sequence of Gloeobacter kilaueensis: looking for another one in metagenomes

The evolution of D1 proteins is complicated. It is characterized by many gene duplication events occurring at every taxonomic level. Some of these duplications could potentially predate the most recent common ancestor of all described cyanobacteria.

See our previous work on this:

Article Origin and Evolution of Water Oxidation before the Last Comm...

Some of the earliest duplications, we suggested, gave rise to the atypical D1 forms, of which we have described three forms. What I have called Group 0, Group 1, and Group 2 D1.

Group 0 is made of a single sequence, found exclusively in the genome of Gloeobacter kilaueensis. G. kilaueensis has additionally 5 standard D1 forms. There may be a D1 fragment encoded in the genome of the early branching Synechococcus sp. PCC 7336, have a look at this:

http://tanaiscience.blogspot.com/2015/10/evolution-of-oxygenic-photosynthesis.html

Group 1 is the super-rogue D1 also known as chlorophyll f synthase (or PsbA4).

Group 2 is the rogue D1: function unknown/unconfirmed.

A recent preprint by Grettenberger et al., described a new type of early branching cyanobacteria, which was named Aurora. The genome of this cyanobacterium was assembled from a metagenome of a microbial mat found in lake Vanda in Antarctica. It is more than 90% complete. This strain seems to be distantly related to Gloeobacter. As far as I understand, it is not clear however if this strain is an early-branching cyanobacterium sister to Gloeobacter, or whether it predates Gloeobacter, being therefore a sister branch to all described cyanobacteria.

This is the preprint:

Preprint Insights into the evolution of oxygenic photosynthesis from ...

Aurura vandensis has a PSII with a subunit composition similar to that of Gloeobacter. Only one D1 was reported in the preprint, and this is a standard form of D1, a Group 4.

Excited by this, I wondered if I could find another Group 0 sequence in the available metagenomes. Another G0, similar to that from G. kilaueensis.

So, I did a BLAST to all JGI environmental metagenomes: these were a total of 12361. I left out metagenomes categorized as “engineered” or “host-associated”.

To do a BLAST in so many metagenomes directly on the JGI site, it is necessary to split the data into sets of maximum 500 metagenomes. That gives 25 sets of metagenomes that needed to be BLASTed.

My query sequence was the very atypical G0 sequence from G. kilaueensis.

In the first set I obtained more than 30000 hits, which must include D1, D2, L, and M subunits; both complete and partial sequences. The cut-off E-value was 1e-5.

None of the 25 sets produced a sequence similar to the G0 sequence. Nothing close to it. The closest identity was 54%, usually to other standard forms of D1. No sequence alignment included the C-terminus, which is kind of special in the G0 sequence. Some of the metagenome sets gave a top hit to super-rogue D1 sequences, but the level of sequence identity between G0 and the other atypical forms is also just over 50%. This makes sense if the phylogenetic tree that we published in the paper above is correct, as it would imply that the G0 sequence is as close to the other atypical sequences, as it is to the standard forms of D1.

This is because we suggested based on the phylogeny of D1, that Group 1 to Group 4 would make a monophyletic group to the exclusion of the G0 sequence. But, phylogenetic trees are susceptible to artifacts, so having more G0 sequences could potentially improve the D1 phylogeny.

Each search for each of the metagenome sets produced more than 30k hits: that means that I could have obtained more than 750k hits in these 12361 metagenomes! But not a second G0 sequence?

I have to say that I did not examine every sequence in detail (of course)… waaay too many. So there may have been a partial sequence close to G0 that did not score high due to its very short length. If there was another G. kialueensis somewhere else I would have expected at least some identical sequences, but nothing at all!

I thought that Gloeobacter was not that uncommon after all:

Article The Primitive Thylakoid-Less Cyanobacterium Gloeobacter Is a...

Would anyone be interested in repeating this search? :)

This is the link to the G0 sequence: https://www.ncbi.nlm.nih.gov/protein/AGY58976.1

Now, with the recent eruption of Kilauea this unique strain of Gloeobacter may have just gone extinct.

Little paper on the evolution of Photosystem I and oxygenic photosynthesis is out now

A short update. The little manuscript detailing the evolution of Photosystem I and the implications for the evolution of oxygenic photosynthesis is now available in the open access journal Heliyon, have a look:

https://www.heliyon.com/article/e00548/

A press release accompanied the paper. Have a look too if interested: https://bit.ly/2FZKXkA

The main conclusion of the paper is that the duplication event that allowed Photosystem I to become a heterodimer occurred long before the most recent common ancestor of cyanobacteria. It is has been hypothesized that the reason why Photosystem I is a heterodimer in oxygenic photosynthesis has to do with oxygen and avoiding reactive oxygen species. So, if the duplication occurred after the evolution of water oxidation to oxygen it would imply that the earliest stages in the evolution of oxygenic photosynthesis appear much early than currently accepted.

The funny thing is that according to my plans, I was hoping for the Photosystem II version of the manuscript to be published first, link below. I have had to experience however everything that is horrible and beautiful about peer-review, and everything in between, in the process. The manuscript is still there fighting its way to freedom:

https://www.biorxiv.org/content/early/2017/09/15/109447

If you like the paper show your support by sharing the preprint or leaving a comment!

Cyanobacteria doing photosynthesis

Photosystem I and the evolution of oxygenic photosynthesis

I want to understand when and how oxygenic photosynthesis originated. Sometime ago I posted an evolutionary analysis of the core proteins of Photosystem II, which is still undergoing peer-review.

Check it out here if you have not seen it already:

https://www.biorxiv.org/content/early/2017/09/15/109447

Basically, all reaction centres are made of a dimer of homologous core proteins. All Type II reaction centres have a heterodimeric core, meaning that each monomer is different. Photosystem II, the water oxidising enzyme, has a core made of D1 and D2. D1 and D2 share slightly under 30% sequence identity and it is in D1 that the manganese cluster that oxidises water to oxygen is located.

It is pretty evident when the sequence and structure of D1 and D2 are compared, that the homodimeric Photosystem II (before the divergence of D1 and D2) was able to do some highly-oxidising photochemistry on both sides. Indeed, it looks like there was some kind of manganese cluster also in the D2 side at some point in time. It has been suggested before that this homodimeric Photosystem II was able to oxidise water. So if I can time when the gene duplication event that led to D1 and D2 happened, then I can have a pretty good idea of when water oxidation appeared for the first time. That is the subject of the above mentioned paper.

Type I reaction centres come in two versions: with homodimeric cores, meaning that the core is made of two copies of the same subunit; or with heterodimeric cores. The homdimeric Type I reaction centres are found only in anoxygenic phototrophs, and the heterodimeric Type I reaction centres are found only in oxygenic phototrophs: Cyanobacteria and photosynthetic eukaryotes. This heterodimeric Type I reaction centre is also known as Photosystem I.

It is hypothesised that the reason why Photosystem I is heterodimeric in oxygenic photosynthesis has something to do with oxygen… and well, there is no other alternative hypothesis that I know of.

The core of Photosystem I is made of two subunits, PsaA and PsaB. They share about 45% sequence identity. So, if oxygen is responsible for the heterodimerisation of Photosystem I; that means that the gene duplication event that led to PsaA and PsaB had to occur AFTER the evolution of water oxidation to oxygen.

That is the subject of the new manuscript:

https://www.biorxiv.org/content/early/2017/11/27/225888

I found out, like it was the case for Photosystem II, that the divergence of PsaA and PsaB is a lot older than anyone could have imagined… from my calculations, I would say that such gene duplication event occurred minimum 3.4 billion years ago, but it is likely much older than that.

Because PsaA and PsaB are more similar to each other than D1 and D2, it would seem as if the gene duplication event that led to PsaA and PsaB occurred long after the gene duplication that led to D1 and D2… but that may not necessarily be the case: that is only an illusion. Each duplication could have followed each other almost immediately: from this perpesctive, it may even be possible that heterodimeric Photosystem I predates heterodimeric Photosystem II, since the latter was oxidising water in a homodimeric form!

One thing that needs to be taken into account is that PsaA and PsaB are each about 730 to 750 amino acids long, while D1 and D2 are only about 360 amino acids long.

So in the case of D1 and D2: 70% sequence divergence is equivalent to about 250 amino acid differences along the entire sequence.

In the case of PsaA and PsaB, 55% sequence divergence is equivalent to about 440 amino acid differences along the entire sequence.

So consider the following example: if we assume that D1, D2, PsaA, and PsaB evolve at exactly the same rate: measured as amino acid substitutions PER POSITION per unit of time... a change of amino acids at 100 positions would take each protein the same amount of time, but in the case of D1 and D2, that would represent a change in sequence identity of 27%; while in PsaA and PsaB it would represent a change of only 13%!

In real life, however, PsaA and PsaB are evolving at a different pace than D1 and D2... but the difference is not huge.

So the fact that the level of sequence identity of PsaA and PsaB is significantly higher than D1 in D2 does not mean that the gene duplication event had to occur much later in Photosystem I than in Photosystem II. It is only an illusion caused by the fact that PsaA and PsaB are much longer than D1 and D2 and by the fact that sequence similarity in percentage is not necessarily the best measurement of sequence divergence.

Therefore, when the rates of evolution are taken into account and if we add to this the significant level of sequence divergence between PsaA and PsaB, it turns out that this gene duplication event happened a lot deeper in time than anyone could have guessed. Nevertheless, it is consistent with my hypothesis that water oxidation originated rapidly after (or at) the origin of photosynthesis, in the very early Archean.

Origin of water oxidation at the divergence of Type I and Type II reaction centres

Introduction

My friends, the way we think about the evolution of photosynthesis is about to change irreversibly.

I want to share with you some awesome stuff regarding the recent structure of the homodimeric Type I reaction centre by Gisriel et al. (2017) and what I think it all means for the origin of oxygenic photosynthesis. Huge thanks to all the authors. I know it must have been an unbelievable effort.

I have had a chance now to play with the structure a bit. What great pleasure! The structure is amazing and I have seen something that intrigues me enormously. Please, keep reading.

This is the link to the paper describing the structure:

http://science.sciencemag.org/content/357/6355/1021.full

This is a link to the pdb files:

https://www.rcsb.org/pdb/explore/explore.do?structureId=5V8K

We need first a bit of background though:

In a recent letter to the editor of the Journal of Molecular Evolution I argued that the peculiar structural characteristics of Photosystem II are better explained if water oxidation originated at the divergence of Type I and Type II reaction centres (Cardona, 2017).

Article Photosystem II is a Chimera of Reaction Centers

What are these peculiar characteristics?

I find quite peculiar that Photosystem II is made of a core, which originated form a Type II reaction centre (D1 and D2) and an antenna, which originated from a Type I reaction centre (CP43 and CP47).

Even more peculiar still is the fact that the CP43 subunit offers a direct ligand to the Mn4CaO5 cluster.

Another peculiar trait about Photosystem II is that D1 and D2 coordinate each a peripheral chlorophyll, ChlZ-D1 and ChlZ-D2. These peripheral chlorophylls and their binding sites are also conserved in Type I reaction centres, but are not found in anoxygenic Type II reaction centres. This means that the most ancestral reaction centre, before the divergence of Type I and Type II, had these peripheral pigments.

The implication of these peculiarities is that an interaction of ancestral Type I and Type II reaction centres is required for the origin of the Mn4CaO5 cluster. A second implication is that this interaction is continuous since the origin of both types of reaction centres, and therefore since very early after the emergence of photosynthesis and the first reaction centres.

So, given the fact that Photosystem II and Photosystem I 'working in series' is the hallmark of oxygenic photosynthesis. And add to this the fact that Photosystem II is a chimera of Type I and Type II reaction centres… it does not take a huge leap forward to think that the initial divergence of both types of reaction centres is actually linked to the origin of water oxidation chemistry.

Think about this for a moment.

This would actually mean that the earliest stages in the evolution of photosynthesis are related to the origin of water oxidation chemistry. In other words, this would mean that oxygenic photosynthesis traces back to the very early stages in the evolution of photochemical reaction centres (Cardona, 2017).

It sounds crazy, right?

Photosystem II and the homodimeric Type I reaction centre

So, what about the homodimeric Type I reaction centre? What about it?

AMAZINGLY, the structure of the homodimeric Type I reaction centre has a Ca-binding site with a number of intriguing parallels to the Mn4CaO5 cluster of Photosystem II:

1. It is positioned exactly where the redox Tyr-His pair is found in D1 and D2 (See Figures 1 and 2).

2. It is connected to the C-terminus by L605 and V608. V608 is the last amino acid in the sequence. In D1 of Photosystem II, the Mn4CaO5 cluster is coordinated by D342 and A344. A344 is the last amino acid of the processed D1 and it ligates not only Mn, but also the Ca!!!!!!!!!

3. It has a connection to the antenna domain, via N263, which is within the 5th and 6th helices. N263 connects to the Ca via two water molecules. In PSII, the CP43 antenna residue E354 offers a ligand to two Mn atoms and it is in the loop connecting the 5th and 6th helices of the antenna! A totally homologous site is also found in D2 and CP47, but phenylalanine residues are found instead of ligands.

4. At the overlapping position where TyrZ/TyrD is, there is a coordinating aspartate.

Figure 1: Panel A shows the Ca-binding site from the reaction centre of H. modesticaldum. In grey I show the connections from the core domain, and in orange the connections from the antenna domain. Panel B shows a schematized version of the Ca-binding site and in italics I have highlighted the parallels with the Mn4CaO5 cluster. In Panel C I show PSII for comparison; and in Panel D I overlap D1 (orange) and PshA (grey). The yellow atom is the Ca of the H. modesticaldum reaction centre.

Figure 2: It shows a comparison of PSII and the homodimeric reaction centre. No doubt that the Ca-binding site and the Mn4CaO5 cluster occupy homologous positions.

Implications for the evolution of water oxidation and the origin of photosynthesis

The main implication is that the most ancestral reaction centre before the divergence of Type I and Type II reaction centres had, at the very least, a Ca-binding site like the one in the structure of H. modesticaldum.

This is strong evidence that the divergence of Type I and Type II reaction centres was due to the development of the structural and energetic requirements to support water oxidation chemistry and the emergence of the oxygen-evolving complex.

This explains why the Mn4CaO5 cluster has a Ca atom! It was there to begin with.

This explains why the Mn4CaO5 cluster has a ligand from the C-terminus. It was there to begin with!

This explains why the Mn4CaO5 cluster has a ligand from the antenna. Guess what? It was there to begin with!

This explains why the site is also mirrored in D2 and CP47, because it all started symmetrically on both sides, as suggested by Rutherford and Faller (2003).

In other words, this implies that the connection from the C-terminus and the antenna domain to the cluster site has been continuous since the emergence of the first reaction centres. Just as I mentioned in my letter!

This also implies that the emergence of water oxidation can be traced to the earliest events in the evolution of photosynthesis. It implies that water oxidation likely predates the diversification of most groups of phototrophs, including Cyanobacteria!

This implies that Cyanobacteria are the only bacteria to have retained water oxidation chemistry, but a greater diversity of oxygenic phototrophs must have predated them.

This is also in perfect agreement with the conclusions of my molecular clock analysis that suggests water oxidation started long before the most recent common ancestor of Cyanobacteria:

Article Molecular evidence for the early evolution of photosynthetic...

(I have uploaded a new version of this article to the BiorXiv (http://www.biorxiv.org/content/early/2017/09/15/109447)

This implies that the anoxygenic Type II reaction centres likely evolved from a water-oxidizing Type II reaction centre before the gene duplication event that led to D1 and D2.

I had mentioned earlier that the ancestral Type II reaction centre (before D1, D2 , L, and M) already had some of the components that were needed to evolve the water-oxidizing complex (Cardona, 2015, 2016; Cardona et al., 2015). This validate those observations too.

In the near future, I hope to write something more substantial about this. Put all these ideas together in a nice review: go a bit deeper. In the meantime, it would be nice to discuss what you all think of this madness!

Don't hesitate to leave comments, especially if you strongly disagree and think this is all bonkers.

References

Cardona, T. (2015). A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res, 126(1), 111-134. doi:10.1007/s11120-014-0065-x

Cardona, T. (2016). Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution? Frontiers in Plant Science, 7, 257. doi:10.3389/fpls.2016.00257

Cardona, T. (2017). Photosystem II is a chimera of reaction centers. Journal of Molecular Evolution, 84(2-3), 149-151. doi:10.1007/s00239-017-9784-x

Cardona, T., Murray, J. W., & Rutherford, A. W. (2015). Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol Biol Evol, 32(5), 1310-1328. doi:10.1093/molbev/msv024

Gisriel, C., Sarrou, I., Ferlez, B., Golbeck, J. H., Redding, K. E., & Fromme, R. (2017). Structure of a symmetric photosynthetic reaction center-photosystem. Science, 357(6355), 1021-1025. doi:10.1126/science.aan5611

Rutherford, A. W., & Faller, P. (2003). Photosystem ii: Evolutionary perspectives. Philos Trans R Soc Lond B Biol Sci, 358(1429), 245-253. doi:10.1098/rstb.2002.1186

2. Results – First phylogeny of BchC and we have discovered a new phototroph!

Phylogeny of BchC

BchC is also known as 3-hydroxyethyl BChlide a dehydrogenase (Bryant et al. 2012). It catalyses the oxidation of the 3-hydroxyethyl group, in the bacteriochlorophyllide a precursor, to a 3-acetyl moiety (Lange et al. 2015).

A pfam search using a BchC from Chloroflexus found that it belongs to the pfam family: “ADH_zinc_N (PF00107)”, or Zinc-binding dehydrogenases.

It is a large family of proteins with more than 50k sequences in the database. That complicates things tremendously, but less not lose courage just yet.

A BLAST in the refseq database showed that all BchC have overall an E-value greater than 7e-29. Some of the more divergent ones appear to be from Proteobacteria.

I used the BchC sequence of Chloroflexus aggregans DSM 9485 as query and made a cut-off at 1000 sequences, excluding eukaryotes. Of these, about 550 are likely true BchC sequences, with the rest being a range of dehydrogenases found in a wide diversity of prokaryotes. I can tell this mostly by doing quick neighbor joining trees of the sequences: but, judging from the E-values, annotations, or by comparing the sequences alone is really hard to tell where BchC sequences end and where other dehydrogenases begin.

The E-value of the 450 ‘other’ dehydrogenases ranged from 1e-28 to 1e-18 relative to my query.

I aligned the 1000 sequences using Clustal Omega and 10 HMM iterations. There was a significant number of gaps and insertions… so there is likely to be some artefacts… but it is preliminary: just to see what the trees look like so far, and to see what type of sequences I have retrieved.

The tree below was calculated using the online service: http://www.atgc-montpellier.fr/phyml/

I used their new Smart Model Selection option with the ‘Bayesian Information Criterion’ (Lefort et al. 2017). This pretty much computes all parameters from the data. You guys are amazing, thanks for making phylogenetics easier to deal with! Double thumbs up for you! I used the NNI tree searching setting and the aLRT SH-like setting for branch support. It ran for nearly 20 hours.

Preliminar ML phylogeny of BchF.

The black dots are supported nodes, above 0.8, and those in yellow have no support. I only added these to key nodes.

I was thinking that the tree was going to reproduce the same phylogeny as BchF (see previous update), but there are a number of differences. I suspect those differences may be the result of artefacts.

You can see that all the BchC are monophyletic, with good support. BchC were split into two groups by the outgroup (grey branches): one includes the Proteobacteria sequences; and the other includes the rest of the photototrophs.

As expected, the BchC of Gemmatimonas branched within the Proteobacteria (Zeng et al. 2014).

I expected that the Acidobacteira branch was going to be sister to Proteobacteria, as in BchF, but instead it clustered with the other ones, but with no support at all. I think this might be a bit of an artefact… Similarly, I expected the sequence from the Chloroflexus to cluster with Acidobacteria and Proteobacteria as sister of the two, but it also branched with low support.

I had retrieved the same topology as BchF in some previous tests I had done with smaller datasets, so there may be some attraction going on here. But who knows… we’ll confirm this later on when I refine the analysis a bit.

It seems that the Chlorobi have two types of BchC, which is interesting because they also have two types of BchF. This may be known already though, not sure about that.

At this point, I don’t want to draw many conclusions on the implications. Unlike, BchF, which do not seem to have homologous in other processes, these dehydrogenases seem to be quite abundant across the tree of life, so it is much harder to make sense of their evolution.

A new group of phototrophs in metagenomic sequences?

For the moment, I want to point out an unusual BchF sequences that branched ‘early’ within the Proteobacteria group. It is coloured orange in the tree. As you can see in the screen captures, that sequence is annotated as belonging to Euryarchaeota Archaeon TMED255 38454, GenBank: NHLA01000022.1.

Photosynthetic Archaea? The gene cluster in the metagenome

The sequence is in a fragement that include 12 other sequences, all of them seem to be from a photosynthesis gene cluster and includes sequences like BchF, BchIDH, BchG, BchXYZ, PufL and PufM. This is unusual because there are no strains of Archaea known to be able to do chlorophyll-based photosynthesis.

I BLASTed the PufL sequence and the best hit was to:

AAM48602.1: photosynthetic reaction center L subunit [uncultured marine proteobacterium], 97% sequence coverage, an E-value of 2e-157, and a level of sequence identity of 77%. It is quite divergent, which means that these sequences originated from a clade of Proteobacteria that has not yet been characterized. Some of the Mg-chelatase subunits in that cluster have a level of sequence identity to the best hit of only about 45%!

BLAST results for PufL in that gene cluster

Lo and behold my friends! We have just discovered a new type of phototroph!

Now, the question is: is this an event of horizontal gene transfer from an uncharacterized clade of phototrophic Proteobacteria into a strain of Archaea, or is it a misannotation, or some sort of contamination? I am not familiar with the intricacies of metagenomics and genome assemblies, so I cannot tell. Can you tell?

If the HGT event is true, we have the first case of a phototrophic Archaea ever discovered! But I think contamination or bad annotation is more likely.

The metagenome project is:

AUTHORS: Tully,B.J., Sachdeva,R., Graham,E.D. and Heidelberg,J.F.

TITLE: 290 Metagenome-assembled Genomes from the Mediterranean Sea: a resource for marine microbiology

JOURNAL Unpublished

I have noted also ChlLNB sequences in two genomes of Altiarchaea, this represents bona fide horizontal gene transfer, but these strains do not have any other photosynthesis genes and they live in subsurface environments. The transfer occurred from another unidentified group of phototrophs. I wrote a short blog-post about this, please take a look of you’re interested: http://tanaiscience.blogspot.co.uk/2017/05/a-new-undiscribed-clade-of-phototrophic.html

References

Bryant, D., Z. Liu, T. LI, F. Zhao, C. G. Klatt, D. Ward, N. U. Frigaard and J. Overmann (2012). Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. Functional Genomics and Evolution of Photosynthetic Systems. R. L. Burnap and W. Vermaas. Dordrecht Springer. 33: 47-102.

Lange, C., S. Kiesel, S. Peters, S. Virus, H. Scheer, D. Jahn and J. Moser (2015). "Broadened Substrate Specificity of 3-Hydroxyethyl Bacteriochlorophyllide a Dehydrogenase (BchC) Indicates a New Route for the Biosynthesis of Bacteriochlorophyll a." Journal of Biological Chemistry 290(32): 19697-19709.

Lefort, V., J. E. Longueville and O. Gascuel (2017). "SMS: Smart Model Selection in PhyML." Molecular Biology and Evolution 34(9): 2422-2424.

Zeng, Y. H., F. Y. Feng, H. Medova, J. Dean and M. Koblizek (2014). "Functional Type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes." Proceedings of the National Academy of Sciences of the United States of America 111(21): 7795-7800.