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Award Abstract # 1536989
Ecological impacts and drivers of double-stranded DNA viral communities in the global oceans

NSF Org: OCE
Division Of Ocean Sciences
Recipient: OHIO STATE UNIVERSITY, THE
Initial Amendment Date: August 27, 2015
Latest Amendment Date: July 16, 2020
Award Number: 1536989
Award Instrument: Standard Grant
Program Manager: Daniel J. Thornhill
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: September 1, 2015
End Date: August 31, 2021 (Estimated)
Total Intended Award Amount: $851,485.00
Total Awarded Amount to Date: $851,485.00
Funds Obligated to Date: FY 2015 = $851,485.00
History of Investigator:
  • Matthew Sullivan (Principal Investigator)
    mbsulli@gmail.com
Recipient Sponsored Research Office: Ohio State University
1960 KENNY RD
COLUMBUS
OH  US  43210-1016
(614)688-8735
Sponsor Congressional District: 03
Primary Place of Performance: Ohio State University
OH  US  43210-1016
Primary Place of Performance
Congressional District:
03
Unique Entity Identifier (UEI): DLWBSLWAJWR1
Parent UEI: MN4MDDMN8529
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1097, 1174, 7308, 8811, 9117
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Ocean microbes produce half of the oxygen that humans breath and drive much of the energy and nutrient transformations that fuel ocean ecosystems. Viruses of microbes alter these microbial impacts through mortality, moving genes from one organism to another, and reprogramming a host cell's metabolism during infection. However, current understanding of ocean viruses is limited to just a few specific model systems or study sites. This project will produce a foundational dataset - the Global Ocean Virome (GOV) - for contextualizing newly discovered viruses, and use this dataset to evaluate the environmental conditions that structure viral communities or how viral communities change over time and space. Additionally, the project will illuminate 'viral dark matter' by experimentally identifying viral structural proteins and generating and investigating single-cell genomic datasets to link novel and abundant viruses to their host cells. The project will train 6 researchers, as well as lead to curriculum, seminars and a public exhibit at The Wellington School and the Columbus Center Of Science and Industry that will together reach approximately 500 students and 250,000 members of the public.

The GOV dataset is comprised of 104 viral metagenomes from around the world's surface and deep oceans. This project seeks to analyze the GOV to identify and quantify viral populations globally, then evaluate these data for ecological patterns to determine the ecological drivers of surface and deep ocean viral community structure. These patterns and drivers will be interpreted in the context of (i) viral metaproteomic experiments to maximally annotate unknown viral proteins that are structural, (ii) paired microbial sequence datasets (metagenomes and metatranscriptomes) that will enable assessment of how biotic factors impact viral community structure and (iii) single-cell amplified genomes and phageFISH experiments that will enable identification of hosts for abundant and novel viruses identified in the GOV. In total, this project will further optimize recently developed genome- and population-based viral ecology methods to establish a first available global map of surface and deep ocean viral populations from both free viromes and infected microbes. These analyses will help evaluate and establish myriad hypotheses about viral roles in marine microbial ecology and biogeochemistry, and the dataset will be a foundational resource for microbial and viral ecologists to contextualize new viruses, identify viruses in microbial datasets, and explore virus-host interactions both phenomenologically and through ecosystem modeling. The GOV will be made publicly available through the NSF-funded iPlant Cyberinfrastructure and metaVIR (http://metavir-meb.univ-bpclermont.fr/).

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Bolduc, B.*, Jang, H.B.*, Doulcier, G., You, Z.Q., Roux, S., Sullivan, M.B. "vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria" PeerJ , v.5 , 2017 , p.3243
Bolduc, B., Youens-Clark, K., Roux, S., Hurwitz, B.L.^, & Sullivan, M.B. "iVirus: facilitating new insights into viral ecology with software and community datasets imbedded in a cyberinfrastructure." The ISME Journal , 2016 doi: 10.1038/ismej.2016.89
Bolduc, B., Youens-Clark, K., Roux, S., Hurwitz, B.L., & Sullivan, M.B. "iVirus: facilitating new insights into viral ecology with software and community datasets imbedded in a cyberinfrastructure" ISMEJ , v.11 , 2017 , p.7
Gregory, Ann C. and Zayed, Ahmed A. and Conceição-Neto, Nádia and Temperton, Ben and Bolduc, Ben and Alberti, Adriana and Ardyna, Mathieu and Arkhipova, Ksenia and Carmichael, Margaux and Cruaud, Corinne and Dimier, Céline and Domínguez-Huerta, Guillermo "Marine DNA Viral Macro- and Microdiversity from Pole to Pole" Cell , v.177 , 2019 10.1016/j.cell.2019.03.040 Citation Details
Howard-Varona, C.*, Hargreaves, K.R.*, Abedon, S.T. & Sullivan, M.B. "Lysogeny in nature ? mechanisms, impact and ecology of temperate phages" ISMEJ , v.16 , 2017 , p.1
Howard-Varona, C., Lindback, M., Bastien, G., Solonenko, N., Zayed, A., Jang, H.B., Andreopoulos, B., Brewer, H., Glavina del Rio, T., Adkins, J., Paul, S., Sullivan, M.B.^, & Duhaime, M.^ "Phage-specific metabolic reprogramming of virocells" The ISME Journal , v.14 , 2020 , p.881
Krzysztof, S., Caputi, L., Buttigieg, P.L., D?Alelio, D., Ibarbalz, F.M., Sullivan, M.B., Chaffron, S., Bowler, C., d?Alcala?, M.R., Iudicone, D. "Modelling plankton ecosystems in the meta-omics era. Are we ready?" Marine Genomics , v.32 , 2017 , p.1
Roux, S., Brum, J.R., Dutilh, B.E., Sunagawa, S., Duhaime, M.B., Loy, A., Poulos, B.T., Solonenko, N., Lara, E., Poulain, J., Pesant, S., Kandels-Lewis, S., Dimier, C., Picheral, M., Searson, S., Cruaud, C., Alberti, A., Duarte, C.M.M., Gasol, J.M.M., "Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses" Nature , v.537 , 2016 , p.689
Roux, S. Solonenko, N. Dang, V.T. Poulos, B.T. Schwenck, S.M. Goldsmith, D.B. Coleman, M.L. Breitbart, M. Sullivan, M.B. "Towards quantitative viromics for both double-stranded and single-stranded DNA viruses" PeerJ , v.4 , 2016 , p.e2777
Vik?, D.R., Roux, S., Brum, J.R., Bolduc, B., Emerson, J.B., Padilla, C.C., Stewart, F.J., Sullivan, M.B. "Putative archaeal viruses from the mesopelagic ocean" PeerJ , v.5 , 2017 , p.3428

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

The oceans represent a source of food, livelihood, and biogeochemical cycling that impacts our everyday lives. On the latter, the oceans absorb human-released carbon dioxide from the atmosphere, having, in effect, approximately halved the climate change impact of these gases. Critical to this ocean ?ecosystem service? are the floating organisms, or plankton, that are comprised of microbes and viruses, which effectively serve as a biological carbon pump on a grand scale. This is because it is these plankton that determine whether the ocean-absorbed atmospheric climate gases are incorporated into biomass and disposed to the deep sea or remineralized and released back into the atmosphere. For this reason, ocean scientists have long studied the organisms that drive the ocean carbon pump to better understand how the oceans will impact climate and the nutrient and energy flows that underpin much of how the Earth System works. In 2008, an ambitious, international project -- the Tara Oceans Expedition -- was launched to systematically study viruses, microbes, and small plants and animals throughout the world?s oceans. 

This NSF-funded project focused on understanding the viruses, and their larger ecosystem roles throughout the Global Ocean. Using methods developed to be portable enough to function on a sailboat (the ?Tara? research vessel) and systematic enough to allow for global sampling, we discovered via sequencing over 200,000 new virus species, which predominantly infect bacteria. Because virtually every one of these viruses were new to science, we developed machine learning approaches to classify them. With this Global Ocean virus catalog, we then identified the most abundant viruses so that they could be studied in the laboratory, as well as in the field. Laboratory experiments of some of the most abundant viruses revealed complex mechanisms of resistance, and how virus infections change under nutrient limitation. Genome sequencing revealed viruses directly encoded genes for photosynthesis, as well as cycling of carbon, nitrogen, and sulfur -- which directly implicates viruses in the very biogeochemical cycles for which the oceans are so important. Most unexpectedly, ecological modeling revealed that of all the plankton community members, viruses best predict the flux of carbon from surface to deep waters in the oceans. This means that viruses likely play an even bigger role in ocean food webs and nutrient cycling than previously realized, and the findings have spurred the field towards new experiments to better understand this.

Beyond the science, which resulted in over 15 research articles including several ?top tier? in Science, Nature, and Cell, this award supported several efforts that will have long-standing impact. First, the Global Ocean Virome dataset developed here serves as a critical resource for researchers around the world that want to study viruses in the oceans. Second, this award supported world-class training and research experience to dozens of undergraduates, graduates, and postdocs, as well as several ?viromics workshops? for workforce training efforts that impacted more than 100 trainees from around the world. Third, students and postdocs were trained in a new generation of ?big team science?, as well as how to communicate in public-facing venues including with the press corps and a science museum. Lastly, to best communicate this novel view of the impact of viruses in natural ecosystems, we collaborated with the Center of Science and Industry (COSI), which is a science museum and research center in Columbus, Ohio, to design and multi-year exhibit showcasing the role, impact, and diversity of viruses in the oceans. The exhibit is set to open to the public in December 2021, and will share the excitement of ?Tara Oceans? science in a way that will impact a large fraction of the >250K annual COSI visitors.


 

 


Last Modified: 11/30/2021
Modified by: Matthew Sullivan

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