The overall goal of this project was to examine how host-virus interactions influence microbial community structure. This project took advantage of Yellowstone hot springs as model systems to link temporal changes in virus abundance and diversity to host genetic and taxonomic diversity. We investigated the hypothesis that chronic viral infections contribute positively to host fitness, increasing the success of the virus-host pair as an evolutionary unit. We hypothesized that these benefits are realized in a highly competitive community context where chronic viruses protect their hosts from future infection and increase their competitive advantage when they act antagonistically against susceptible competitors and that viruses play a direct role in maintaining microbial diversity by exerting a combination of antagonistic and commensal effects on the fitness of their host populations.  This study contributed to our understanding of the role of viruses in dictating the ecology and evolution of natural systems, at the level of community composition, function and stability.

This project resulted in both significant intellectual merit and broader impacts outcomes. The major scientific findings include the following. First, this project established a comprehensive temporal understanding of all of the major viruses present in the study hot springs. A total of 110 virus types were identified, most of which were new viruses to science. We determined that the presence of these viruses was relatively stable within a given hot spring over the 5-year study time of this project.  At the same time, we were measuring viruses within hot springs, we determined the composition of the cellular microbial community. For example, we determined that the cellular microbial community of one hot spring consisted of only 8 cellular members (7 archaeal and 1 bacterial).  To our knowledge, this is the most comprehensive and complete temporal virus and cellular host inventory for any natural environment, providing an excellent system for examining host-virus associations in detail in an ecological context.  Second, once we had established at the community population level both the cellular and viruses members, we linked the viruses community to the cellular community. This was accomplished by the development of two techniques; single cell genomics of hot spring samples and the development of a combined cellular and viral florescence in situhybridization assay (vFISH). The results of this work showed most (all) cells were interacting with viruses and that many cells may be interacting multiple viruses simultaneously.  Third, we determined what viruses were likely actively replicating in a given cell and the possible nature of their association with the cell (e.g. lytic, lysogenic, or chronic infections). This was accomplished by examining virus replication at the transcript level (RNA expression). We estimated that while all three viral lifestyles are present, that chronic infections are quite common. Fourth, catalyzed by this finding of non-lytic viral strategies, we developed a theoretical framework to analyze the fitness of viruses of microbes across a continuum from lysis to chronic to latent.  The theory unifies disparate classes of virus-microbe dynamics and provides a rationale for ecological regimes that non-lytic interactions. Fifth, field studies were complemented by laboratory-based experiments aim at isolation and genetic characterization of both hot spring cells and their viruses. These studies led to the discovery and characterization of previously unknown archaeal viruses and the discovery of new mechanisms of virus assembly. Likewise, characterization of cellular hosts led to the discovery of a viral defense strategy, termed distributed immunity, that operates on a population level to limit pathogenic virus within the microbial community while supporting the maintenance of non-pathogenic viruses. Finally, the results of this project have been placed in ecological/evolutionary context by the modeling of host-virus dynamics that allows their broad use in understanding host-virus interactions in diverse natural environments.

The broader impacts component of this project were significant. This included the further development and implementation of Project Microbe, a multi-day education program directed at middle and high school science teachers to enhance their understanding and teaching us microbiology within their classrooms. This course was taught nationally and even attracted science teachers from other countries.  Likewise, Yellowstone-based field trips were developed for training middle and high school teachers to learn about environmental microbiology in natural environments and how environmental microbiology can be incorporated into their classrooms. These one-week field course were exceptionally popular and attracted teachers from around the country and overseas. Finally, Yellowstone-based ‘Exploration Days’ were developed that took middle and high school kids into Yellowstone for a day long course in environmental microbiology.  

Last Modified: 01/14/2019
Modified by: Mark J Young