Metabolic reprogramming by viruses in the sunlit and dark ocean

Bonnie L Hurwitz,Steven J Hallam,Matthew B Sullivan

doi:10.1186/gb-2013-14-11-r123

Bonnie L Hurwitz, Steven J Hallam + Show 1 more

Open Access

https://doi.org/10.1186/gb-2013-14-11-r123

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Abstract

BackgroundMarine ecosystem function is largely determined by matter and energy transformations mediated by microbial community interaction networks. Viral infection modulates network properties through mortality, gene transfer and metabolic reprogramming.ResultsHere we explore the nature and extent of viral metabolic reprogramming throughout the Pacific Ocean depth continuum. We describe 35 marine viral gene families with potential to reprogram metabolic flux through central metabolic pathways recovered from Pacific Ocean waters. Four of these families have been previously reported but 31 are novel. These known and new carbon pathway auxiliary metabolic genes were recovered from a total of 22 viral metagenomes in which viral auxiliary metabolic genes were differentiated from low-level cellular DNA inputs based on small subunit ribosomal RNA gene content, taxonomy, fragment recruitment and genomic context information. Auxiliary metabolic gene distribution patterns reveal that marine viruses target overlapping, but relatively distinct pathways in sunlit and dark ocean waters to redirect host carbon flux towards energy production and viral genome replication under low nutrient, niche-differentiated conditions throughout the depth continuum.ConclusionsGiven half of ocean microbes are infected by viruses at any given time, these findings of broad viral metabolic reprogramming suggest the need for renewed consideration of viruses in global ocean carbon models.

Highlights

Marine ecosystem function is largely determined by matter and energy transformations mediated by microbial community interaction networks
Ruling out bacterial contamination in viromes Given the need to differentiate between bona fide viral Auxiliary metabolic gene (AMG) and low-level cellular DNA contamination, all viromes were prepared from prefiltered (
It is improbable that DNA would survive such processing without the protection of a protein capsid, it is not possible to exclude gene transfer agents (GTAs, which randomly package host DNA and co-purify with viral particles [30]) or cellular DNA contamination, without additional post-processing of genomic sequence information

Summary

Introduction

Marine ecosystem function is largely determined by matter and energy transformations mediated by microbial community interaction networks. Marine ecosystems exert a profound influence on the operating conditions for life on earth [1,2], and their function is largely determined by matter and energy transformations flowing through microbial interaction networks [3,4] Viral infection modulates these network properties through mortality, gene transfer, and metabolic reprogramming. Emerging evidence supports a general model of viral reprogramming in which perturbations in glycolysis, the pentose phosphate pathway (PPP), and the tricarboxylic acid (TCA) cycle alter the metabolic flux and energy homeostasis of the host cell in support of viral replication and propagation at different stages of infection [17,18,19] Environmental studies extend this concept to include cyanophages, as enhanced metabolic flux through the PPP increases production of NADH and ribose 5phosphate, driving deoxynucleotide biosynthesis for phage replication [20]

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