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Viruses inhibit CO2 fixation in the most abundant phototrophs on Earth

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Richard J. Puxty, Andrew D. Millard, David John Evans, David J. Scanlan

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Abstract

Summary. 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 × 1027 [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.
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Original languageEnglish
Pages (from-to)1585-1589
Number of pages6
JournalCurrent Biology
Volume26
Issue number12
Early online date9 Jun 2016
DOIs
StatePublished - 20 Jun 2016

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