Thursday, January 15, 2015

The origin of oxygenic photosynthesis in Cyanobacteria (some thoughts)


The last common ancestor to all extant cyanobacteria had already evolved the capability to oxidize water as the earliest known diverging species of cyanobacteria of the genus Gloeobacter have a fully evolved Photosystem II. For example, Gloeobacter violaceous has five D1, D2, the CP43 and CP47, the Cyt b559, Cyt c550, PsbO, L, M, J, K, H, T, X, and P [1-3].

It can be deduced with confidence that oxygenic photosynthesis evolved before the last common ancestor of extant cyanobacteria. It suggests a period of evolution that saw the transformation of a simple Type II reaction center incapable of water oxidation into the sophisticated Photosystem II.

The question is: for how long before the last common ancestor of extant cyanobacteria was water oxidation possible? Could water oxidation by a primitive Photosystem II have evolved fast?

The Great Oxygenation Event occurred around 2.3-2.4 Ga ago. I think this time correspond to the major radiation of cyanobacteria… when the major clade of cyanobacteria evolved, but after the evolution of the Gloeobacter genus and early evolving Synechococcus (e.g. Yellowstone strains).

The closest relatives of cyanobacteria that are incapable of oxygenic photosynthesis are the melainabacteria [4, 5]. It appears though, oxygenic photosynthesis appeared some time in between the divergence of the melainabacteria and the last common ancestor of the cyanobacteria. Before this, there is the divergence of the chloroflexi from the lineage that led to cyanobacteria [6]. Because the chloroflexi are phototrophs I dare to suggest that the chloroflexi and the cyanobacteria shared a photosynthetic ancestor that was incapable of water oxidation [7].

Based on molecular clock analysis it’s been estimated that the major phyla of bacteria radiated around 3.2 Ga [8, 9].

Some of the earliest evidence for oxygen on earth date to ~3.0 Ga [10, 11].

So, I speculate that there is about 200 million years for water oxidation to have evolved, starting from the major radiation of bacteria and culminating with the first significant amounts of oxygen detected in the geochemical record.

Evidence of oxygenic photosynthesis before 3.2 Ga… are difficult to reconcile with the overall evolution of bacteria. IF for some unexpected reason strong evidence for oxygenic photosynthesis around 3.8 Ga is found. This should imply panspermia… maybe a rock containing a huge diversity of prokaryotes with all sorts of archaea and bacteria (including fully evolved cyanobacteria) hit earth during the late heavy bombardment. But I don’t think that makes much sense given the available evidence :-)

GOE great oxyganation event
Sequence of events in the evolution of water oxidation

1. Saw, J.H.W., et al., Cultivation and Complete Genome Sequencing of Gloeobacter kilaueensis sp nov., from a Lava Cave in Kilauea Caldera, Hawai'i. Plos One, 2013. 8(10).

2. Koyama, K., et al., Oxygen evolution in the thylakoid-lacking cyanobacterium Gloeobacter violaceus PCC 7421. Biochim Biophys Acta, 2008. 1777(4): p. 369-78.

3. Kaneko, T., et al., Complete genome structure of the unicellular cyanobacterium Gloeobacter violaceus PCC 7421. Plant and Cell Physiology, 2004. 45: p. S129-S129.

4. Soo, R.M., et al., An Expanded Genomic Representation of the Phylum Cyanobacteria. Genome Biology and Evolution, 2014. 6(5): p. 1031-1045.

5. Di Rienzi, S.C., et al., The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife, 2013. 2.

6. Segata, N., et al., PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nature Communications, 2013. 4.

7. Cardona, T., A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res, 2014.Advanced access, 18 of Dec.

8. David, L.A. and E.J. Alm, Rapid evolutionary innovation during an Archaean genetic expansion. Nature, 2011. 469(7328): p. 93-96.

9. Battistuzzi, F.U. and S.B. Hedges, A major clade of prokaryotes with ancient adaptations to life on land. Molecular Biology and Evolution, 2009. 26(2): p. 335-343.

10. Crowe, S.A., et al., Atmospheric oxygenation three billion years ago. Nature, 2013. 501(7468): p. 535-8. 11. Planavsky, N.J., et al., Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nature Geosci, 2014. 7(4): p. 283-286.

Tuesday, January 13, 2015

Reflexions on the origin of photochemical reaction centers

My review paper dealing with the evolution of photosynthesis has been published now in Photosynthesis Research. Please, take a look:

A fresh look at the evolution and diversification of photochemical reaction centers

Phylogenetic tree of prokaryotes