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Energy limitation of cyanophage development : implications for marine carbon cycling

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Puxty_2018_ISME_Cyanophagedevelopment_CC.pdf (1.101Mb)
Date
05/2018
Author
Puxty, Richard J.
Evans, David J.
Millard, Andrew D.
Scanlan, David J.
Keywords
QR Microbiology
Microbiology
Ecology, Evolution, Behavior and Systematics
NDAS
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Abstract
Marine cyanobacteria are responsible for ~25% of the fixed carbon that enters the ocean biosphere. It is thought that abundant co-occurring viruses play an important role in regulating population dynamics of cyanobacteria and thus the cycling of carbon in the oceans. Despite this, little is known about how viral infections ‘play-out’ in the environment, particularly whether infections are resource or energy limited. Photoautotrophic organisms represent an ideal model to test this since available energy is modulated by the incoming light intensity through photophosphorylation. Therefore, we exploited phototrophy of the environmentally relevant marine cyanobacterium Synechococcus and monitored growth of a cyanobacterial virus (cyanophage). We found that light intensity has a marked effect on cyanophage infection dynamics, but that this is not manifest by a change in DNA synthesis. Instead, cyanophage development appears energy limited for the synthesis of proteins required during late infection. We posit that acquisition of auxiliary metabolic genes (AMGs) involved in light-dependent photosynthetic reactions acts to overcome this limitation. We show that cyanophages actively modulate expression of these AMGs in response to light intensity and provide evidence that such regulation may be facilitated by a novel mechanism involving light-dependent splicing of a group I intron in a photosynthetic AMG. Altogether, our data offers a mechanistic link between diurnal changes in irradiance and observed community level responses in metabolism, i.e., through an irradiance-dependent, viral-induced release of dissolved organic matter (DOM).
Citation
Puxty , R J , Evans , D J , Millard , A D & Scanlan , D J 2018 , ' Energy limitation of cyanophage development : implications for marine carbon cycling ' , ISME Journal , vol. 12 , no. 5 , pp. 1273-1286 . https://doi.org/10.1038/s41396-017-0043-3
Publication
ISME Journal
Status
Peer reviewed
DOI
https://doi.org/10.1038/s41396-017-0043-3
ISSN
1751-7362
Type
Journal article
Rights
© The Author(s) 2018. This article is published with open access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Description
RJP was in receipt of a Natural Environment Research Council (NERC) PhD studentship and a Warwick University IAS Fellowship. This work was also supported in part by NERC grant NE/N003241/1 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/10023/12692

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