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Exploring the Vast Diversity of Marine Viruses by Mya Breitbart, Luke R This article has This been published in or collective redistirbution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The approval portionthe ofwith any permitted articleonly photocopy by is machine, of this reposting, means or collective or other redistirbution A S E A O F M I C ROB E S > SecTION V. EXAMPleS OF DIveRSITY Oceanography > CHAPTER 10. MICROBIAL COmmUNITIES > A . WATER COLUMN , Volume 20, , Volume Exploring the Vast Diversity of Marine Viruses N BY MYA BREITBART, LUKE R . THOMPSON, CURTIS A . SUTTle, AND MATTHEW B. SUllIVAN umber 2, a quarterly journal of journal The umber 2, a quarterly At abundances routinely greater than Here, we review advances in understand- high. Mathematical modeling based on 10 million particles per milliliter, viruses ing viral diversity and genome evolution, viral metagenomic data predicts that are the most numerous biological and discuss potentially fruitful areas there are hundreds of thousands of viral O ceanography ceanography entities1 in the oceans. To put the sheer for future research. Our emerging view genotypes in the world’s ocean (Angly abundance of marine viruses in context, of the virosphere, inferred from giga- et al., 2006). This may not be surprising S we note that they contain more carbon bases of sequence data ground truthed given that marine microbial prokaryotic ociety. Copyright 2007 by The 2007 by Copyright ociety. than 75 million blue whales and, if such by model systems in culture, is one of and eukaryotic diversity is also enor- viruses were joined end-to-end, they would stretch further than the nearest 60 galaxies (Suttle, 2005). While marine ...65–95% of marine viral metagenomic viruses were first described by Spencer O sequences are not similar to previously ceanography ceanography O (1955), they were largely ignored for ceanography ceanography three decades because of the relatively described sequences, as opposed to ~ 10% S ociety. ociety. low abundances inferred using culture- for cellular metagenomic surveys. S ociety. ociety. based assays. However, since Bergh et al. A ll rights reserved. S (1989) recognized their numeric impor- end all correspondence to: [email protected] or Th e [email protected] to: all correspondence end tance, they have been considered at least immense but finely tuned genetic diver- mous (e.g., Irigoien et al., 2004; Witman as abundant as marine microbes, and sity, where viruses have seemingly end- et al., 2004; Thompson et al., 2005; P ermission is granted to copy this article for use in teaching and research. article use for research. and this copy in teaching to granted is ermission scientists have been characterizing them less genetic potential, yet clearly are Worden, 2006), and there are likely to and trying to determine the extent of maintaining key genetic elements to be multiple host-specific viruses infect- marine viral diversity. Extensive efforts propagate their extraordinary success. ing each marine organism (Moebus, have focused on understanding the role One focus area is the diversity of 1991; Moebus, 1992; Waterbury and of viruses in horizontal gene transfer and marine viruses and marine viral com- Valois, 1993; Wilson et al., 1993; Wichels microbial mortality, and on the conse- munities. Although viruses might defy et al., 1998; Sullivan et al., 2003). The O ceanography ceanography quent impacts on microbial abundance, traditional species concepts, it is clear diversity of marine viral morpholo- diversity, and community structure. that viral genetic diversity is extremely gies ranges from a variety of icosahe- S ociety, ociety, dral tailed phages (Figure 1) (Moebus, PO MYA BREITBART ([email protected]) is Assistant Professor, College of Marine Science, 1991; Moebus, 1992; Waterbury and B ox 1931, ox University of South Florida, St. Petersburg, FL, USA. LUKE R. THOMPSON is Ph.D. Candidate, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, 1 Viruses themselves are nonmetabolic (outside of the R ockville, MD 20849-1931, R epublication, systemmatic reproduction, reproduction, systemmatic epublication, USA. CURTIS A. SUTTle is Professor, Departments of Earth & Ocean Sciences, Botany, infection process) and lack the standard genetic marker (ribosomal RNA) that allows routine genetic compari- and Microbiology & Immunology, University of British Columbia, Vancouver, Canada. son of known and unknown life forms using the “Tree of MATTHEW B. SUllIVAN is Postdoctoral Associate, Department of Civil and Environmental Life,” so they are often not considered “alive.” The term “biological entities” is used to allow classification of Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA. viruses with other life forms. USA . Oceanography June 2007 135 diversity in natural communities is enor- mous and dynamic as revealed at the levels of morphology, single genes, and whole genome sizes. Recently, genomic sequencing of marine viral isolates and metagenomic sequencing of marine viral communi- ties has revealed a plethora of previ- ously unknown viruses. Among cul- tured marine phage genomes, typically between 60% and 80% of the open reading frames show no similarity to any sequences in GenBank (Paul and Sullivan, 2005), while some marine viruses infecting protists have almost no recognizable similarity to extant sequences (Nagasaki et al., 2005b). Furthermore, 65–95% of marine viral Figure 1. Electron micrographs of representative ocean cyanobacterial viruses that infect Prochlorococcus metagenomic sequences are not simi- and Synechococcus. Panels A and B represent the noncontracted and contracted tails of myoviruses, lar to previously described sequences respectively. Note that the tails are nonflexible and contain rather conspicuous baseplates and tail fibers. Panels C, D, and E represent siphoviruses that contain long, flexible, noncontractile tails. Note the vari- (Breitbart et al., 2002, 2004; Angly et al., ability in tail length, tail-terminus structures, and capsid morphology in C and D as compared to E. 2006; Culley et al., 2006), as opposed to Panel F shows the icosahedral capsids of podoviruses that contain small, noncontractile tails. All black ~ 10% for cellular metagenomic surveys scale bars are 100 nm. Photos by M.B. Sullivan, P. Weigele, and B. Ni. Images C and D were originally pub- lished in Sullivan et al. (2006) (Tyson et al., 2004; Venter et al., 2004), suggesting that we have only begun to scratch the surface of marine viral sequence diversity. Valois, 1993; Proctor, 1997; Wichels et virus HcRNAV [Nagasaki et al., 2005a] One of the most striking features of al., 1998; Sullivan et al., 2003) to long and the 407 kb Coccolithovirus HeV-86 this sequence diversity is an abundance filamentous viruses (Middelboe et al., [Wilson et al., 2005]). Studies target- of viral-encoded genes that were previ- 2003) with particle diameters ranging ing genes conserved among members ously thought to be restricted to cellular from 25 nm (Schizochytrium single- of a viral group (e.g., g20 and g23 of genomes with metabolic capacity. For stranded RNA virus SssRNAV) (Takao myophages [Fuller et al., 1998; Zhong example, photosynthesis genes, which et al., 2005) up to ~ 300 nm for a virus et al., 2002; Marston and Sallee, 2003; would seem of little use to something that infects a marine phagotrophic pro- Filee et al., 2005; Short and Suttle, other than a photosynthetic cell, are tist (Garza and Suttle, 1995). Reported 2005], the RNA polymerase of picorna now thought to be common in cyano- marine viral genome sizes range from viruses [Culley et al., 2003], or the DNA phages (Mann et al., 2003; Lindell et al., 4.4 kilobases (kb) (Tomaru et al., 2004) polymerase of algal viruses [Chen et 2004; Millard et al., 2004; Sullivan et to 630 kb (Ovreas et al., 2003), with al., 1996; Short and Suttle, 2002] and al., 2006). Extensive sequencing efforts representative genome sequences avail- T7-like podophages [Breitbart and on these core photosystem II reaction- able from cultured isolates from nearly Rohwer, 2004]) demonstrate tremendous center genes show that cyanophages the extremes of the observed ranges single-gene diversity even within these themselves act as genetic reservoirs for (the 4.4 kb Heterocapsa circularisquama restricted groups of viruses. Thus, viral their hosts, generating diversity even at 136 Oceanography Vol. 20, No. 2 the level of these globally distributed across multiple phage lineages, such as the role of viruses in host metabolism genes (Zeidner et al., 2005; Sullivan et the photosynthesis and carbon metabo- is perhaps even more important. It is al., 2006). Gene-expression studies on lism genes, which suggest that these now recognized that marine viruses rou- model phage-host pairs show that both genes play critical roles during infection, tinely procure AMGs to tap into critical, messenger RNA (Lindell et al., 2005; likely augmenting biochemical processes rate-limiting steps of host metabolism Clokie et al., 2006) and protein (Lindell at key metabolic bottlenecks (Figure 2). during infection (Sullivan et al., 2006; et al., 2005) are produced from viral For this reason, we suggest the term Angly et al., 2006). Such AMGs are not photosynthesis genes during infection, “auxiliary metabolic genes” (AMGs) random evolutionary noise, but rather which suggests that they are functional. rather than the potentially misleading entrenched parts of viral genomes, akin Several other so-called “host genes,” term “host genes” when describing
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