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Energy limitation of cyanophage development: implications for marine carbon cycling

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Energy limitation of cyanophage development : implications for marine carbon cycling. / Puxty, Richard J.; Evans, David J.; Millard, Andrew D.; Scanlan, David J.

In: ISME Journal, Vol. 12, No. 5, 05.2018, p. 1273-1286.

Research output: Contribution to journalArticle

Harvard

Puxty, RJ, Evans, DJ, Millard, AD & Scanlan, DJ 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

APA

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, 12(5), 1273-1286. https://doi.org/10.1038/s41396-017-0043-3

Vancouver

Puxty RJ, Evans DJ, Millard AD, Scanlan DJ. Energy limitation of cyanophage development: implications for marine carbon cycling. ISME Journal. 2018 May;12(5):1273-1286. https://doi.org/10.1038/s41396-017-0043-3

Author

Puxty, Richard J. ; Evans, David J. ; Millard, Andrew D. ; Scanlan, David J. / Energy limitation of cyanophage development : implications for marine carbon cycling. In: ISME Journal. 2018 ; Vol. 12, No. 5. pp. 1273-1286.

Bibtex - Download

@article{f0cfe6f1edb1440998e21b1b74336c21,
title = "Energy limitation of cyanophage development: implications for marine carbon cycling",
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).",
author = "Puxty, {Richard J.} and Evans, {David J.} and Millard, {Andrew D.} and Scanlan, {David J.}",
note = "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.",
year = "2018",
month = "5",
doi = "10.1038/s41396-017-0043-3",
language = "English",
volume = "12",
pages = "1273--1286",
journal = "ISME Journal",
issn = "1751-7362",
publisher = "Nature publishing group",
number = "5",

}

RIS (suitable for import to EndNote) - Download

TY - JOUR

T1 - Energy limitation of cyanophage development

T2 - ISME Journal

AU - Puxty, Richard J.

AU - Evans, David J.

AU - Millard, Andrew D.

AU - Scanlan, David J.

N1 - 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.

PY - 2018/5

Y1 - 2018/5

N2 - 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).

AB - 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).

U2 - 10.1038/s41396-017-0043-3

DO - 10.1038/s41396-017-0043-3

M3 - Article

VL - 12

SP - 1273

EP - 1286

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 5

ER -

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