Viruses Inhibit CO2 Fixation in the Most Abundant Phototrophs on Earth.
Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most numerous photosynthetic organisms on our planet [1, 2]. With a global population size of 3.6 × 10(27) [3], they are responsible for approximately 10% of global primary production [3, 4]. Viruses that infect Prochlorococcus and Synechococcus (cyanophages) can be readily isolated from ocean waters [5-7] and frequently outnumber their cyanobacterial hosts [8]. Ultimately, cyanophage-induced lysis of infected cells results in the release of fixed carbon into the dissolved organic matter pool [9]. What is less well known is the functioning of photosynthesis during the relatively long latent periods of many cyanophages [10, 11]. Remarkably, the genomes of many cyanophage isolates contain genes involved in photosynthetic electron transport (PET) [12-18] as well as central carbon metabolism [14, 15, 19, 20], suggesting that cyanophages may play an active role in photosynthesis. However, cyanophage-encoded gene products are hypothesized to maintain or even supplement PET for energy generation while sacrificing wasteful CO2 fixation during infection [17, 18, 20]. Yet this paradigm has not been rigorously tested. Here, we measured the ability of viral-infected Synechococcus cells to fix CO2 as well as maintain PET. We compared two cyanophage isolates that share different complements of PET and central carbon metabolism genes. We demonstrate cyanophage-dependent inhibition of CO2 fixation early in the infection cycle. In contrast, PET is maintained throughout infection. Our data suggest a generalized strategy among marine cyanophages to redirect photosynthesis to support phage development, which has important implications for estimates of global primary production.
School of Life Sciences, University of Warwick, West Midlands CV4 7AL, UK; Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA 92697, USA.
Richard J
RJ
Puxty
Warwick Medical School, University of Warwick, West Midlands CV4 7AL, UK.
Andrew D
AD
Millard
Biomedical Sciences Research Complex, North Haugh, University of St Andrews, Fife KY16 9ST, UK.
David J
DJ
Evans
School of Life Sciences, University of Warwick, West Midlands CV4 7AL, UK. Electronic address: d.j.scanlan@warwick.ac.uk.
David J
DJ
Scanlan
D001435:Bacteriophages / Q000254:growth & development*; D057486:Carbon Cycle; D004579:Electron Transport; D020387:Food Chain; D054884:Host-Pathogen Interactions; D010788:Photosynthesis; D010839:Phytoplankton / Q000378:metabolism / Q000821:virology; D046940:Synechococcus / Q000378:metabolism / Q000821:virology*