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Viruses inhibit CO2 fixation in the most abundant phototrophs on Earth

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Evans_2016_CurrBiol_CO2Fixation_CC.pdf (686.2Kb)
Date
20/06/2016
Author
Puxty, Richard J.
Millard, Andrew D.
Evans, David John
Scanlan, David J.
Keywords
QH301 Biology
NDAS
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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.
Citation
Puxty , RJ , Millard , AD , Evans , D J & Scanlan , DJ 2016 , ' Viruses inhibit CO 2 fixation in the most abundant phototrophs on Earth ' , Current Biology , vol. 26 , no. 12 , pp. 1585-1589 . https://doi.org/10.1016/j.cub.2016.04.036
Publication
Current Biology
Status
Peer reviewed
DOI
https://doi.org/10.1016/j.cub.2016.04.036
ISSN
0960-9822
Type
Journal article
Rights
© 2016 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Description
R.J.P. was the recipient of a NERC studentship and Warwick University IAS fellowship. This work was supported in part by NERC grant NE/J02273X/1 and Leverhulme Trust grant RPG-2014-354 to A.D.M., D.J.E., and D.J.S.
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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/9025

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