Viruses: unlocking the greatest biodiversity on Earth

It is a great pleasure to be here, and I want to thank the organizers for giving me an opportunity to tell you about some of our results and ideas. The last two talks were a great introduction to the focus of my talk, biodiversity; I want to discuss how little we know. There are three objectives to my talk. First, most of you will not have heard about viruses in the context that I wish to discuss them today; I want to make the case that most of the biodiversity on the planet is actually found in viruses. Second, I want to convince you of the importance of viruses other than as purveyors of disease, and that if it were not for viruses, life on the planet would probably not exist, or at least we would not exist. Third, I wish to show how genomics is the lens through which we can unlock this diversity and potentially make some remarkable discoveries along the way. This is a symposium about genomics, the power and the promise. The power, of course, is that genomics is allowing us to unlock this diversity. New sequencing technologies are uncovering diversity we never knew existed. The promise is that this diversity has untold riches, that we will be able to use for all kinds of things including understanding how ecosystems function. We heard some nice stories about what diversity represents, but not what is meant by biodiversity. I work in the Beaty Biodiversity Research Centre, and a definition that resonates with me and many of my colleagues is that biodiversity is the totality of genes, species, and ecosystems in a region. In 1992, this definitionwas agreed upon by the United Nations Environment Program, Global Biodiversity Strategy, after a large round of consultations. Obviously, if there is no genetic diversity, there is no biodiversity. Species richness ultimately stems from the underlying genetic diversity, which underpins ecosystem richness and diversity. Ultimately, the roots of biological diversity and ecosystem function reside in the overall genetic diversity. In the context ofmarine biological diversity, our understanding of the oceans has changed markedly. Originally, the seas were seen only as a resource to exploit, whether it was simply as an avenue to transport goods or as a fishery. More recently, the oceans are being viewed as a vast reservoir of potential genetic and biological diversity that can be interrogated to uncover processes and functions. Perhaps surprising to some, most life in the oceans, by weight, is microbial. In fact, if on one side of a giant balance you could place everything microscopic (the protists, bacteria, archaea, and viruses) and on the other side you placed the things that people can see (the fish, whales, algae, crustacean, zooplankton, etc.), 95% to 98% of the living material, by weight, in the oceans is microscopic. This invisible majority not only produces half the oxygen on the planet, but if we think about biodiversity, ecosystem functioning, or biogeochemical cycles, we need to think about the microbial life in the seas. Almost all of the life in the oceans, by weight, is prokaryotic (bacteria and archaea), with viruses and protists making up roughly equal amounts of the remaining. The big stuff, the whales and other charismatic megafauna are actually pretty trivial in terms of overall biomass. There are about 200megatonnes of carbon in viruses in the ocean,which is equal to about 75 million blue whales. The most biomass that was ever in whales, as far as we know, was about 13 megatonnes. These numbers are dwarfed by the carbon in prokaryotes, which is about 5.2 gigatonnes. As I tell my students, whales are great; many are top predators; however, if you are interested in how the planet functions, it is not the whales that are important, it is the microbial life that we cannot see. If we look at life by numbers, it is different. There are about 10 times as many viruses in the oceans as there are bacteria and about 1000-fold less protists than bacteria. In fact, in a litre of coastal seawater there are more viruses than there are people on the planet. If one takes a drop of seawater and adds a nucleic-acid stain such as Yo-Pro, SYBR Green, or SYBR Gold and looks at it under a microscope, there are a myriad of tiny fluorescent dots that are reminiscent of a clear night sky (Fig. 1). Most of these dots are virus particles. If aliens randomly sampled Earth they would see a planet dominated by microbial life, most of which would be viruses. On average, there are about 10 million viruses and a million bacteria per litre of seawater or freshwater. If we compare the number of viruses in the oceans to the number of stars in the universe, there are about 1023 stars in the universe. In contrast, there are about 10 million-fold more viruses in the ocean than there are stars in the universe. If we took the 1030 viruses in the oceans and stretched them end-to-end, how far would they go? Assuming, the average length of a virus is about 100 nm, the viruses would stretch 1023 m, which is 1020 km. If converted to light years, by dividing by 1013 km, we end upwith 10million light years. The nearest star is Proxima Centauri, about 4.2 light years away; the Crab Supernova is 1000 light years away; our own galaxy, the Milky Way, is about 150 000 light years across. In fact, all the viruses in the ocean end-to-endwould stretch further than the nearest 60 galaxies. This may seem like a trivial calculation, but it is important on a number of levels. For one reason, these viruses are responsible for about Avogadro’s number, about 1024 infections per second in the ocean. Each one of these events is an opportunity for lateral transfer of genes. Most of the genetic information on Earth probably resides within viruses. The number of viruses in the sea is enormous, but why does anybody care? As mentioned before, 95% to 98% of the biomass in the ocean is in microbes, which produce about half of the oxygen on the planet. Moreover, viruses kill about 20% of the living material in the ocean every day; hence, viruses are incredibly important in driving global cycles. Earlier concepts that the flow of the ocean’s living resources goes from phytoplankton to zooplankton to fish have to be modified to incorporate the viral shunt, which