Ocean viruses and their effects on microbial communities and biogeochemical cycles
School of Biology, Georgia Institute of Technology, Atlanta GA 30332-0230, USA
School of Physics, Georgia Institute of Technology, Atlanta GA 30332-0230, USA
Department of Microbiology, University of Tennessee-Knoxville, Knoxville, TN 37996-0845, USA
The electronic version of this article is the complete one and can be found at: http://f1000.com/reports/b/4/17
Viruses are the most abundant life forms on Earth, with an estimated 1031 total viruses globally. The majority of these viruses infect microbes, whether bacteria, archaea or microeukaryotes. Given the importance of microbes in driving global biogeochemical cycles, it would seem, based on numerical abundances alone, that viruses also play an important role in the global cycling of carbon and nutrients. However, the importance of viruses in controlling host populations and ecosystem functions, such as the regeneration, storage and export of carbon and other nutrients, remains unresolved. Here, we report on advances in the study of ecological effects of viruses of microbes. In doing so, we focus on an area of increasing importance: the role that ocean viruses play in shaping microbial population sizes as well as in regenerating carbon and other nutrients.
The study of viruses of microbes has undergone a revolution in the past 20 years. What has been termed “The Third Age of Phage”  can be viewed more broadly as a renewal of interest in environmental viruses, and in particular in viruses of microbes [2-11]. This renewal has been spurred by advances in direct-imaging methods, sequencing technologies and bioinformatics that have revealed a previously unknown world of viral diversity in natural environments . The study of viruses in the oceans has been key to many discoveries: from the finding that viruses have evolved novel lineages of key photosynthetic genes (as in cyanophages infecting Synechococcus and Prochlorococcus [13-17]) to the identification of many novel viral families that defy much of the conventional wisdom about viral life history (e.g. the discovery of “giant” algal-infecting viruses [18,19] and even viruses that exploit other viruses ). Altogether, it is well established that a diverse reservoir of viruses infect and lyse bacteria, archaea and microeukaryotes at the base of the ocean's food web [2,21]. Despite the growing literature on viruses of microbes, we remain relatively poorly informed concerning the dynamic, ecological effects of virus infection of marine microbes. In this report, we focus on the functional role of viruses within oceanic waters. In doing so, we highlight knowns, unknowns and challenges in three areas: (i) the role of ocean viruses in shaping microbial community composition; (ii) the role of ocean viruses in determining carbon and nutrient availability; (iii) modelling efforts to link viral infection of microbes with ecosystem-scale consequences.
Viral infection and microbial community composition
Viruses, in general, and viruses of microbes, in particular, infect a subset of available hosts in any environment. The subset of hosts that a virus typically infects is narrower than the range of microbes that are typically consumed by a grazer species (e.g. a protist or zooplankton). However, there is evidence that viruses of microbes can infect hosts from different species or even different genera. For example, some cyanophages can infect different strains within the same cyanobacteria species, either Synechococcus or Prochlorococcus, as well as strains of different cyanobacterial genera . The quantitative study of the host-range of viruses of microbes is in its infancy [22-26], an issue we return to later. Successful viral infections can lead to lysis of hosts as well as the conversion of hosts into lysogens where the viral genome is integrated into that of the host, subsequently altering host physiology [2,21,27]. Lytic viral infection of microbes and its effects are our primary concerns here.
Viral lysis of microbes is thought to have direct effects