Marine Viral Ecology Laboratories
at the University of Hawaiʻi at Mānoa
We are a collective of two lab groups in the Department of Oceanography that collaborate to understand the diversity and ecological consequences of viral infections of marine plankton using theoretical and empirical approaches.
MarVEL Team Members
Kyle Edwards
Associate Professor
Grieg Steward
Professor
Julie Thomy
Post-doctoral Researcher
Anamica Bedi de Silva
Graduate Student
Andrian Gajigan
Graduate Student
Petra Byl
Graduate Student
Kelsey McBeain
Research Staff
Amanda Laughlin
Graduate Student
Learn more about our virus work and our other research interests at our individual lab group pages:
Theoretical and experimental plankton ecology - mathematical approaches to ecological systems
Viruses of phytoplankton, bacteria, & archaea - ecology, diversity, biogeochemical consequences
What are viruses?
Viruses are mobile genetic elements that differ from other such elements in having an extracellular form known as a virion. In the simplest form, a virion consists of the viral nucleic acid (the viral genome) packaged in a protein shell (capsid), but some types of viruses produce more complex virions with lipid membranes or protein appendages. No matter how complex, virions are not metabolically active and are not capable of growth or division, they are primarily vessels for delivery of the virus' nucleic acid—and sometimes some enzymes— to the interior of a cell. If the viral genome enters the appropriate type of cell (a host), the cell's metabolic machinery, along with any machinery provided by the virus, will act on the information encoded in the genome to either replicate the viral genome as a genetic element within the cell or facilitate the assembly of new virions that exit the cell (usually killing the cell in the process). The first viruses likely arose together with the very first cells billions of years ago and have been co-evolving and diversifying with cells ever since. Others viruses likely had more recent, independent origins. The long history and multiple origins of viruses makes this an extraordinarily diverse suite of elements linked by a common general mode of replication.
Why study marine viral ecology?
Every organism on our planet, from the largest whale to the tiniest bacterium, has evolved under the influence of, and remains susceptible to, infection by viruses. Viruses are perhaps best classified as molecular symbionts of cells with relationships that range from mutualistic to parasitic. As a mutualism, a virus' genome is stably replicated and maintained within the cell and, in return, the expression of select viral genes provides the host cell with some benefit. In this mode, a virus alters the phenotype, and thus the ecological function, of the host cell. These mutually beneficial interactions are likely common among viruses and plankton in the ocean, but examples and mechanisms remain poorly documented. Better studied and understood are the examples of parasitism, in which a virus replicates within a cell, creating new virions at the expense of cell fitness. Most often the cell is lysed to release the newly assembled virions in the manner of a parasitoid. Viruses are one of the major contributors to plankton death in the ocean and, as a consequence, seawater is teeming with virions, often numbering in the tens of billions per liter. Because infections spread most readily through dense populations, and because viruses are specific in which types of cells they infect, infections are thought to disproportionately kill members of dominant populations. This equalizing effect from antagonistic virus-host interactions can promote diversity in marine microbial communities and drive succession of dominant populations. In habitats with persistently high or persistently low cell concentrations, selection may instead favor stable mutualistic relationships between viruses and their hosts. The many profound and complex interactions between viruses and their hosts and the extraordinary breadth of viral diversity that remains to be discovered make this one of the most exciting and challenging research areas in the marine sciences.
Recent Virus-related Publications
(visit our individual lab sites for full list of publications on all topics)
DeLong JP, Al-Sammak MA, Al-Ameeli ZT, Dunigan DD, Edwards KF, Fuhrmann JJ, Gleghorn JP, Li H, Haramoto K, Harrison AO, Marston, MF, Moore RM, Polson SW, Ferrell BD, Salsberry ME, Schvarcz CR, Shirazi J, Steward GF, Van Etten J, Wommack KE (2021) Toward an integrative view of virus phenotype. Nature Reviews Microbiology doi: https://doi.org/10.1038/s41579-021-00612-w
Arisdakessian C, Nigro OD, Steward GF, and Belcaid M (2021) CoCoNet: An Efficient Deep Learning Tool for Viral Metagenome Binning. Bioinformatics, btab213, DOI: 10.1093/bioinformatics/btab213
Edwards KF, Steward GF, Schvarcz CR (2020) Making sense of size and the tradeoffs shaping viral fitness. Ecology Letters 24: 363-373. https://doi.org/10.1111/ele.13630
Kukovetz K, Hertel B, Schvarcz CR, Saponaro A, Manthey M, Burk U, Greiner T, Steward GF, Van Etten J, Moroni A, Thiel G, Rauh O (2020) A functional K+ channel from Tetraselmis virus 1, a member of the Mimiviridae. Viruses 2020, 12 (10), 1107; doi:10.3390/v12101107 (access online)
Roux S, Adriaenssens EM, Dutilh BE, Koonin EV, Kropinski AM, Krupovic M, Kuhn JH, Lavigne R, Brister JR, Varsani A, Amid C, Aziz RK, Bordenstein SR, Bork P, Breitbart M, Cochrane GR, Daly RA, Desnues C, Duhaime MB, Emerson JB, Enault F, Fuhrman JA, Hingamp P, Hugenholtz P, Hurwitz BL, Ivanova NN, Labonté JM, Lee K-B, Malmstrom RR, Martinez-Garcia M, Mizrachi IK, Ogata H, Páez-Espino D, Petit M-A, Putonti C, Rattei T, Reyes A, Rodriguez-Valera F, Rosario K, Schriml L, Schulz F, Steward GF, Sullivan MB, Sunagawa S, Suttle CA, Temperton B, Tringe SG, Thurber RV, Webster BS, Whiteson KL, Wilhelm SW, Wommack KE, Woyke T, Wrighton KC, Yilmaz P, Yoshida T, Young MJ, Yutin N, Allen LZ, Kyrpides NC, Eloe-Fadrosh EA (2019) Minimum information about an uncultivated virus genome (MIUVIG) Nature Biotechnology 37(1):29-37 (access online).
Schvarcz CR, Steward GF (2018) A giant virus infecting green algae encodes key fermentation genes Virology 518: 423-433 (access online).
Edwards KF, Steward GF (2018) Host traits drive viral life histories across phytoplankton viruses The American Naturalist 191(5) 566-581 (access online).
Nigro OD, Jungbluth SP, Lin H-T, Hsieh C-C, Miranda JA, Schvarcz CR, Rappé MS, Steward GF (2017) Viruses in the oceanic basement MBio 8(2): e02129-16 (access online).
Miranda JA, Steward GF (2017) Variables influencing the efficiency and interpretation of reverse transcription quantitative PCR (RT-qPCR): An empirical study using Bacteriophage MS2. Journal of Virological Methods 241:1-10 (access online).
Miranda JA, Culley AI, Schvarcz CR, Steward GF (2016) RNA viruses as major contributors to Antarctic virioplankton. Environmental Microbiology 18(11) 3714-3727 (access online).
Culley AI, Mueller JA., Belcaid M, Wood-Charlson EM, Poisson G, Steward GF (2014). The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. MBio 5(3):e01210-14 (access online).
Mueller JA, Culley AI, Steward GF (2014) Variables influencing extraction of nucleic acids from microbial plankton (viruses, bacteria, and protists) collected on nanoporous aluminum oxide filters. Applied Environmental Microbiology 80(13):3930-3942 (access online).
Brum JR, Culley AI, Steward GF (2013) Assembly of a marine viral metagenome after physical fractionation. PLoS One 8(4): e60604. doi:10.1371/ journal.pone.0060604 (access online).
Steward GF, Culley AI, Wood-Charlson EM (2013) Marine Viruses, in: Levin, S. (Ed.), Encyclopedia of Biodiversity. Academic Press, Waltham. (request reprint).
Steward GF, Culley AI, Mueller JA, Wood-Charlson EM, Belcaid M, Poisson G. (2012). Are missing half of the viruses in the ocean? ISME doi: 10.1038/ismej.2012.121 (access online).
Nigro OD, Culley AI, Steward GF (2012) Complete genome sequence of bacteriophage VvAW1, which infects Vibrio vulnificus. Standards in Genomic Sciences 6: 415-426. doi:10.4056/sigs.2846206. (view online).
Steward GF, Preston CM (2011) Analysis of a viral metagenomic library from 200 m depth in Monterey Bay, California constructed by direct shotgun cloning. Virology Journal 8: 287 (doi: 10.1186/1743-422X-8-287) (access online). A link to the metagenome in MG-RAST is here: http://metagenomics.anl.gov/metagenomics.cgi?page=MetagenomeOverview&metagenome=4461422.3
Brum JR, Steward GF (2011) Physical fractionation of aquatic viral assemblages. Limnology and Oceanography: Methods 9: 150-163 (link to abstract).
Brum JR, Steward GF (2010) Morphological characterization of viruses in the stratified water column of alkaline, hypersaline Mono Lake. Microbial Ecology 60(3): 636-643 Download.
Culley AI, Suttle CA, Steward GF (2010). Characterization of the diversity of marine RNA viruses, pp. 193-201. In: Wilhelm, S.W., Weinbauer, M.G., and Suttle, C.A. (eds.) Manual of Aquatic Viral Ecology. ASLO. (Link to book online).
Lawrence JL, Steward GF (2010). Purification of viruses by centrifugation. pp. 166-181. In: Wilhelm, S.W., Weinbauer, M.G., and Suttle, C.A. (eds.) Manual of Aquatic Viral Ecology. ASLO. (Link to book online).
Steward GF, Culley AI (2010) Extraction and purification of nucleic acids from viruses. pp. 154-165. In: Wilhelm, S.W., Weinbauer, M.G., and Suttle, C.A. (eds.) Manual of Aquatic Viral Ecology. ASLO. (Link to book online).
Lang AS, Culley AI, Rise ML, Steward GF (2009) RNA viruses in the sea. FEMS Microbiology Reviews. 33(2): 295-332. DOI: 10.1111/j1574-6976.2008.00132.x (PDF).
Culley AI, Asuncion BF, Steward GF (2009) Detection of inteins among diverse DNA polymerase genes of uncultivated members of the Phycodnaviridae. ISME 3(4): 409-418 (PDF).
Culley AI, Steward GF (2007) New genera of RNA viruses in subtropical seawater inferred from polymerase gene sequences. Applied and Environmental Microbiology 73(18): 5937-5944 (PDF).
Steward GF, Fandino LB, Hollibaugh JT, Whitledge TE, Azam F (2007) Microbial biomass and viral infections of prokaryotes in the mid-waters of the central Arctic Ocean. Deep-Sea Research I 54(10): 1744-1757 (PDF).
Workman M, Nigro OD, Steward GF (2006) Identification of prophages in coastal water isolates of Staphylococcus aureus. Journal of Young Investigators 15 (PDF).
Brum JR, Steward GF, Jiang S, Jellison R (2005) Spatial and Temporal variability of prokaryotes, viruses, and viral infections of prokaryotes in an alkaline, hypersaline lake. Aquatic Microbial Ecology 41: 247-260 (PDF).
Steward GF (2005) Viruses in Mono Lake Mono Lake Newsletter 17 (2): 7 (PDF).
Brum JR, Steward GF, Karl DM (2004) A novel method for the measurement of dissolved deoxyribonucleic acid in seawater Limnology and Oceanography: Methods 2: 248-255 (PDF).
Jiang SC, Steward GF, Jellison R, Chu W, Choi S (2004) Abundance, distribution and diversity of viruses in alkaline, hypersaline, Mono Lake, California. Microbial Ecology 47: 9-17 (PDF).
Middelboe M, Riemann L, Steward GF, Hansen V, Nybroe O (2003) Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquatic Microbial Ecology 33(1): 1-10 (PDF).
Noble RT, Steward GF (2001) Estimating viral proliferation in aquatic samples. In: Paul, J.H. (Ed.), Marine Microbiology. Academic Press, Ltd., London, pp. 67-84.
Steward GF (2001) Fingerprinting viral assemblages by pulsed field gel electrophoresis. In: Paul, J.H. (Ed.), Marine Microbiology. Academic Press, Ltd., London, pp. 85-103 (PDF).