Schematic overview diagram of biological process known as photosynthesis.

 

As many of us know, oxygen makes up around 20% of the gas in the atmosphere and is essential for plant and animal life. The human body cannot withstand more than a couple of minutes without an adequate oxygen supply. Green plants, algae, and a group of bacteria known as cyanobacteria (sigh-anno-bact-er-i-ah) are responsible for maintaining atmospheric oxygen levels. Without them, the life-sustaining oxygen we need would not be available.

Around 3 billion years ago, a biological process known as photosynthesis arose within the cyanobacteria. In photosynthesis, light energy from the sun is used to fuel a complex set of chemical reactions in which carbon dioxide and water are turned into sugars and free oxygen. For the cyanobacteria, oxygen was a waste product which was released as a gas into the atmosphere. Over the course of another billion years, this cyanobacterial waste built up in the atmosphere and transformed the Earth into a place suitable for the evolution of plant and animal life. Today, about half of the oxygen needed to sustain the atmospheric pool comes from land plants and the other half comes from cyanobacteria in the ocean.

 

Micrographs of cyanobacteria. Filamentous cyanobacteria (A & B). Unicellular cyanobacteria (C & D). Images A-C were taken with a light microscope. Image D is a thin slice of unicellular cyanobacteria taken with a transmission electron microscope, which shows the internal structure of a cyanobacterial cell. Scale bar size is noted in picture. Photos courtesy of Dr. Ralf Wagner.

We have known for some time that, just like the cells of our bodies, a cyanobacterial cell can be infected and killed by a virus. Over the years, a number of cyanobacterial viruses, also known as cyanophage, have been isolated and studied by scientists around the world. Cyanophages can only infect cyanobacteria and are harmless to any other life forms. Scientists are particularly interested in cyanophages, precisely because their hosts, the cyanobacteria are at the base of the marine food web. Besides producing oxygen, cyanobacteria serve as an important direct food source for larger microorganisms. Eventually, through the many layers of the marine food web, cyanobacterial biomass supports the growth of larger organisms such as fish. Thus, cyanophages, by killing cyanobacteria, actually limit an important source of food and oxygen from the ocean.

Transmission electron micrographs of cyanophage P-SSM2 with its tail extended (A) and contracted (B). Scale bar = 0.1 µm. Photo courtesy of Matt Sullivan.

 

So how does a cyanophage help us breathe if it kills the very cells that produce half the world’s oxygen? In 2003, Professor Nick Mann and co-workers at the University of Warwick in the United Kingdom determined the entire genetic sequence (also known as the genome) of a cyanophage affectionately named S-PM2 (3). To their surprise, the S-PM2 genome contained two genes which encoded the instructions to make the two main proteins of the photosystem II reaction center. Initially, Dr. Mann and his colleagues were confused by this finding as viruses are generally thought to be unable to carry out a metabolic process as complicated as photosynthesis. Moreover, S-PM2 did not contain any of the myriad of other genes necessary for a fully functioning photosynthetic system. Work to unravel the mystery of "cyanophage photosynthesis" began in earnest.

Two years later in 2005, Dr. Debbie Lindell and co-workers at the Massachusetts Institute of Technology discovered that the photosystem II genes of another cyanophage known as P-SSP7 were active during infection and replaced the host cell photosystem II proteins (2). In essence, the cyanophage’s photosystem genes serve to maintain photosynthetic activity, while the virus replicates. Through this strategy of carrying photosynthesis genes the cyanophage prevents the host from stopping viral replication by shutting down photosynthesis through the destruction of the photosystem II reaction center. As it turns out, this strategy has been very successful. Dr. Matt Sullivan now at the University of Arizona, discovered that a number of different cyanophages carry photosynthesis genes (4, 5). Work by my lab group, which was led by Shellie Bench, found that photosynthesis genes were among the most common genes within virioplankton (viral plankton) of the Chesapeake Bay (1).

So the question remains: how much oxygen do cyanophages produce during infection and eventual lysis of cyanobacteria? Current estimates are that around 20% of cyanobacterial cells are killed each day by a cyanophage. If we assume, based on data from the Chesapeake Bay, that half of all cyanophages carry photosynthesis genes, then 10% of all cyanobacteria are killed by a "photosynthetic" cyanophage. We know that half (50%) of all the oxygen in the atmosphere is produced by cyanobacteria, so 50% X 10% = 5%. There’s the answer, 5% of all the oxygen in the atmosphere is actually produced by cyanophage!

As you are breathing, just think that one out of every 20 life-sustaining breaths of oxygen your body consumes comes from a cyanophage infecting a cyanobacteria in the wide open ocean!

Learn more about this fascinating science topic in these publications:

1.   Bench, S. R., T. E. Hanson, K. E. Williamson, D. Ghosh, M. Radosovich, K. Wang, and K. E. Wommack. 2007. Metagenomic characterization of Chesapeake Bay virioplankton. Appl Environ Microbiol 73:7629-41.
2.   Lindell, D., J. D. Jaffe, Z. I. Johnson, G. M. Church, and S. W. Chisholm. 2005. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86-9.
3.   Mann, N. H., A. Cook, A. Millard, S. Bailey, and M. Clokie. 2003. Marine ecosystems: Bacterial photosynthesis genes in a virus. Nature 424:741-741.
4.   Sullivan, M. B., D. Lindell, J. A. Lee, L. R. Thompson, J. P. Bielawski, and S. W. Chisholm. 2006. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4:e234.
5. Molloy, S. 2006. Environmental microbiology: Photosynthetic mix and match. Nature Reviews Microbiology Research Highlights http://www.nature.com/nrmicro/journal/v4/n9/full/nrmicro1501.html