Viruses are small, non-living infectious agents that replicate only inside the cells of living organisms. They can infect all forms of life from plants to animals and even bacteria. Viruses that infect only bacteria are called bacteriophages, or phages. A phage can either kill its’ microbial host or alter the host’s genome by adding genetic material, sometimes functional genes. Because microbes are important players in the cycling of earth’s chemical nutrients such as carbon, oxygen, and nitrogen, this phage-host interaction is important to study. Our focus is on phages in marine environments. It is estimated that there are greater than 1 million viral particles in a milliliter of sea water, yet little is known about these viruses. We work to understand how these tiny but abundant biological entities impact global biogeochemical cycles.
Ocean viruses shape microbial populations and processes through mortality, gene transfer, and metabolic reprogramming. However, quantifying viral roles in nature has been limited by technical challenges. This project sought to develop a quantitative sample-to-sequence metagenomic pipeline for ocean viruses, and more broadly to develop new ways to “see” and understand viruses both in the laboratory and in nature. On the former, a replicated metagenomic experimental design was used to evaluate existing and new methods for concentrating, purifying and sequencing ocean viral DNA. On the latter, diverse approaches were explored. These include developing new phage-host model systems (e.g., Cellulophaga and Pseudoalteromonas) and advancing more well-established ones (e.g., population genomics of cyanophages), as well as developing new methods to link viruses to their hosts either one cell at a time (e.g., phageFISH) or en masse at a population scale (e.g., viral tagging). Further methods were also developed to each quantitatively characterize viral morphology in complex ocean communities (quantitative transmission electron microscopy, qTEM) and to bring annotation to unknown viral sequence space through experimentally determining virion structural proteins in isolates and in nature using (meta)proteomics. Many of these new data types required parallel advances in analytics and visualization strategies which we strive to make accessible through our lab website and well-documented supporting information. Together these advances should lead to better measurements and understanding of an important, but understudied component of the Earth System, the ocean viruses.
Allers, E., C. Moraru, M. B. Duhaime, E. Beneze, N. Solonenko, J. Barrero-Canosa, R. Amann, & M. B. Sullivan. (2013). Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses. Environ Microbiol, 15(8), 2306-2318. doi: 10.1111/1462-2920.12100
Brum, J. R., R. O. Schenck, & M. B. Sullivan. (2013). Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J, 7(9), 1738-1751. doi: 10.1038/ismej.2013.67
Deng, L., A. Gregory, S. Yilmaz, B. T. Poulos, P. Hugenholtz, & M. B. Sullivan. (2012). Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. MBio, 3(6). doi: 10.1128/mBio.00373-12
Duhaime, M. B., L. Deng, B. T. Poulos, & M. B. Sullivan. (2012). Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method. Environ Microbiol, 14(9), 2526-2537. doi: 10.1111/j.1462-2920.2012.02791.x
Duhaime, M. B., & M. B. Sullivan. (2012). Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology, 434(2), 181-186. doi: 10.1016/j.virol.2012.09.036
Holmfeldt, K., D. Odic, M. B. Sullivan, M. Middelboe, & L. Riemann. (2012). Cultivated single-stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA-binding stains. Appl Environ Microbiol, 78(3), 892-894. doi: 10.1128/AEM.06580-11
Holmfeldt, K., N. Solonenko, M. Shah, K. Corrier, L. Riemann, N. C. Verberkmoes, & M. B. Sullivan. (2013). Twelve previously unknown phage genera are ubiquitous in global oceans. Proc Natl Acad Sci U S A, 110(31), 12798-12803. doi: 10.1073/pnas.1305956110
Hurwitz, B. L., L. Deng, B. T. Poulos, & M. B. Sullivan. (2013). Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics. Environ Microbiol, 15(5), 1428-1440. doi: 10.1111/j.1462-2920.2012.02836.x
Hurwitz, B. L., & M. B. Sullivan. (2013). The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology. PLoS One, 8(2), e57355. doi: 10.1371/journal.pone.0057355.t001
Ignacio-Espinoza, J. C., & M. B. Sullivan. (2012). Phylogenomics of T4 cyanophages: lateral gene transfer in the 'core' and origins of host genes. Environ Microbiol, 14(8), 2113-2126. doi: 10.1111/j.1462- 2920.2012.02704.x
Ignacio-Espinoza, J.C., S. A. Solonenko, & M. B. Sullivan. (2013). The global virome: not as big as we thought? Curr Opin Virol, 3(5), 566-571. doi: 10.1016/j.coviro.2013.07.004
Solonenko, S.A., J. C. Ignacio-Espinoza, A. Alberti, C. Cruaud, S. J. Hallam, K. T. Konstantinidis, G. W. Tyson, P. Wincker, & M. B. Sullivan. (2013). Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics, 14(320). doi: 10.1186/1471-2164-14-320
Sullivan, M. B., K. H. Huang, J. C. Ignacio-Espinoza, A. M. Berlin, L. Kelly, P. R. Weigele, A. S. DeFrancesco, S. E. Kern, L. R. Thompson, S. Young, C. Yandava, R. Fu, B. Krastins, M. Chase, D. Sarracino, M. S. Osburne, M. R. Henn, & S. W. Chisholm. (2010). Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol, 12(11), 3035-3056. doi: 10.1111/j.1462-2920.2010.02280.x.
Weitz, J. S., T. Poisot, J. R. Meyer, C. O. Flores, S. Valverde, M. B. Sullivan, & M. E. Hochberg. (2013). Phage-bacteria infection networks. Trends Microbiol, 21(2), 82-91. doi: 10.1016/j.tim.2012.11.003
Zhao, Y., B. Temperton, J. C. Thrash, M. S. Schwalbach, K. L. Vergin, Z. C. Landry, M. Ellisman, T. Deerinck, M. B. Sullivan, & S. J. Giovannoni. (2013). Abundant SAR11 viruses in the ocean. Nature, 494(7437), 357-360. doi:10.1038/nature11921
UA News reports on Eastern Tropical North Pacific Ocean research sampling cruise.
UA News and Science Daily report on the findings of the PNAS Homlfeldt et al. article: Twelve previously unknown phage genera are ubiquitous in global oceans.
UA News reports on the findings of the Nature Zhao et al. publication: Abundant SAR11 viruses in the ocean.
UA News reports on Tara Ocean research sampling cruise.
Watch "Innocence by Viral Tagging," produced for the Ocean 180 Video Challenge:
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