Elucidating marine virus ecology through a unified heartbeat.

Abstract

Marine environments teem with viruses. They are not only the most abundant (109 to 1010 virus l−1) and diverse biological entities in the oceans, but their parasitic lifestyles collectively turn over >25% of global photosynthetically fixed carbon through cell lysis, fuel upper ocean respiration by channeling dissolved organic matter to heterotrophic bacteria, and drive the tempo of microbial evolution by catalyzing the exchange of genetic material (1, 2). In these contexts, viruses are the great engines of oceanic biogeochemistry and microbial evolution. Unfortunately, methodological limitations and the rapid “mosaic” nature of virus evolution (3) have significantly hindered our understanding of virioplankton biology and ecology. Marine viruses come in an astounding array of morphologies, lifestyles, genome organization, and sizes, ranging from the immense nucleocytoplasmic large double-stranded (ds)DNA-containing viruses (NCLDVs), which contain the Pandoraviruses [with up to 2.5-Mb genomes (4)], to the extremely small single-stranded (ss)DNA and RNA representatives characterized by only three to four genes and ∼0.3% the relative genome size [∼1.7–11 Kb (5⇓–7)]. Microbial autotrophs and heterotrophs alike fall prey to this parasitic pressure, with a majority of marine viruses targeting bacteria (bacteriophages) as high abundance targets (109 L−1). Unlike the cellular life of eukarya, bacteria, and archaea, for which universally shared small subunit ribosomal RNA genes have revolutionized our understanding of cellular diversity, ecology, and evolution (8), viruses lack a universally conserved phylogenetic marker. PCR-based approaches have historically targeted specific genes within particular virus subclades [e.g., DNA polymerase genes for viruses infecting eukaryotic microalgae (9) or genes encoding the major capsid protein (g23) of T4-like myoviruses (10)]. “Omic” approaches have since provided unprecedented insight into virus diversity and even a glimpse into inferred function (11), but infection lifestyles have remained elusive given most virus-derived sequences have no database matches (12 … [↵][1]1Email: bidle{at}marine.rutgers.edu. [1]: #xref-corresp-1-1