Award: OCE-1233760

In the oceans, viruses are both highly abundant and diverse, e.g., there are typically over a 10 billion viruses in a liter of surface seawater. Yet the vast majority of these viruses don?t make humans sick. Instead, most of these viruses infect ocean microbes. This NSF Biological Oceanography project led by Joshua Weitz (Professor of Biological Sciences, Georgia Tech), set out to understand how viruses affect life and biogeochemistry in the global oceans. Specifically, this project enabled a multi-year effort to understand which microbes get sick by which viruses, how microbes and viruses persist, and how ocean ecosystems respond to infections taking place at the base of the ocean?s food web. Via collaboration with researchers in the USA and internationally, we characterized datasets and models of cross-infection and their consequences. First, we expanded upon earlier reports that viruses are not just specialists. That is, viruses can infect many more than one type of bacteria. Similarly, bacteria can be infected by many more than one type of virus. Through a systematic network approach, we identified patterns of cross-infection that can be found in highly disparate communities. This cross-infectivity raises the question: which "strategy" is favored, i.e., is it evolutionarily favorable to be a specialist or a generalist for viruses? We found that the answer is context-dependent. We also developed models to show how such cross-infection could persist given trade-offs between infecting hosts vs. persisting in the oceans outside hosts. Yet the consequences of viral infection has many indirect effects. When a virus kills a microbial cell, the remains of the cell may be consumed by other microbes. This is known as the "viral shunt" in the sense that carbon and other nutrients are shunted away from larger organisms that move material up the food chain. In this project, we developed quantitative models of the elemental content and requirements of viruses. As a consequence, we were able to develop a quantitative, mechanistic model revealing how viruses may kill individual cells but indirectly enhance productivity of the community. Collaborating with Steven Wilhelm (UT-Knoxville) and others, we also contested the paradigm that there are 10 viruses per microbe in the ocean. Instead, by re-analyzing data from multiple oceanic expeditions, we found that the average number of viruses per microbe tends to decreases in environments with more microbes. The analysis of virus-microbe interactions and their consequences was enabled by development of computational models and simulations. In the latter stages of the project we developed a community resource tool, BiMAT, to facilitate analysis of interaction networks, including those between viruses and microbes. This tool is available as an open-source library for the community. In addition, all other models in the project, including a new approach to infer networks from time series data, were released via the Weitz group?s GitHub page. The contributions within and between disciplines was facilitated by the contributions of multiple undergraduate and graduate students. Two REU students were supported in the project. In addition, three Ph.D. students were partially supported by this grant. All three graduated with Ph.D.-s in Physics, albeit with application to the biology of virus-host interactions in the oceans. Two of these students moved directly into industry. One is now a postdoctoral fellow. In total, 10 new peer-reviewed articles were published as a direct result of support enabled by this project. The research discoveries in this project directly facilitated a series of efforts that resulted in broader impacts. First, leveraging discoveries and insights, Joshua Weitz wrote a 360 page monograph on Quantitative Viral Ecology. This book was published in December 2015 by Princeton University Press and was awarded the 2016 Best Postgraduate Textbook Prize from the Royal Society of Biology (London, UK). The book includes multiple chapters underlying the quantitative study of virus-microbe interactions and their consequences, as well as capstone chapters focusing on ocean viruses. In addition, Weitz collaborated with Steven Wilhelm (UT-Knoxville) to co-author a perspective on Ocean Viruses published in the New Scientist in 2013. Weitz and his group have also been active in presenting their research in US universities, at international institutions, disciplinary conferences (like the Aquatic Viral Workshop), to conferences focusing on other disciplines (like the American Physical Society annual meeting), and to the general public. Of note, Weitz was the featured speaker in the September 2016 "Atlanta Science Tavern" event on the theme of "Microbes Get Sick, Too". Last Modified: 04/30/2017 Submitted by: Joshua S Weitz