Original Article

Subject Category: Integrated genomics and post-genomics approaches in microbial ecology

The ISME Journal (2014) 8, 1089–1100; doi:10.1038/ismej.2013.216; published online 5 December 2013

Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition

Nana Yaw D Ankrah1, Amanda L May2, Jesse L Middleton2, Daniel R Jones1, Mary K Hadden1, Jessica R Gooding2, Gary R LeCleir1, Steven W Wilhelm1, Shawn R Campagna2 and Alison Buchan1

  1. 1Department of Microbiology, University of Tennessee, Knoxville, TN, USA
  2. 2Department of Chemistry, University of TN, Knoxville, TN, USA

Correspondence: A Buchan, A Buchan, Department of Microbiology, University of Tennessee, M409 WLS, Knoxville, TN 37996-1600, USA. E-mail: abuchan@utk.eduor SR Campagna, Department of Chemistry, University of Tennessee, 618 Buehler Hall, Knoxville, TN 37996-1600, USA. E-mail: campagna@ion.chem.utk.edu

Received 5 April 2013; Revised 27 October 2013; Accepted 31 October 2013
Advance online publication 5 December 2013

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Abstract

Viruses contribute to the mortality of marine microbes, consequentially altering biological species composition and system biogeochemistry. Although it is well established that host cells provide metabolic resources for virus replication, the extent to which infection reshapes host metabolism at a global level and the effect of this alteration on the cellular material released following viral lysis is less understood. To address this knowledge gap, the growth dynamics, metabolism and extracellular lysate of roseophage-infected Sulfitobacter sp. 2047 was studied using a variety of techniques, including liquid chromatography–tandem mass spectrometry (LC-MS/MS)-based metabolomics. Quantitative estimates of the total amount of carbon and nitrogen sequestered into particulate biomass indicate that phage infection redirects ~75% of nutrients into virions. Intracellular concentrations for 82 metabolites were measured at seven time points over the infection cycle. By the end of this period, 71% of the detected metabolites were significantly elevated in infected populations, and stable isotope-based flux measurements showed that these cells had elevated metabolic activity. In contrast to simple hypothetical models that assume that extracellular compounds increase because of lysis, a profile of metabolites from infected cultures showed that >70% of the 56 quantified compounds had decreased concentrations in the lysate relative to uninfected controls, suggesting that these small, labile nutrients were being utilized by surviving cells. These results indicate that virus-infected cells are physiologically distinct from their uninfected counterparts, which has implications for microbial community ecology and biogeochemistry.

Keywords:

marine biogeochemistry; virus infection; bacterial physiology; metabolomics