Award Abstract # 1829831
Ecology and biogeochemical impacts of DNA and RNA viruses throughout the global oceans

NSF Org: OCE
Division Of Ocean Sciences
Recipient: OHIO STATE UNIVERSITY, THE
Initial Amendment Date: August 14, 2018
Latest Amendment Date: August 14, 2018
Award Number: 1829831
Award Instrument: Standard Grant
Program Manager: Cynthia Suchman
csuchman@nsf.gov
 (703)292-2092
OCE
 Division Of Ocean Sciences
GEO
 Directorate For Geosciences
Start Date: August 15, 2018
End Date: July 31, 2022 (Estimated)
Total Intended Award Amount: $1,052,917.00
Total Awarded Amount to Date: $1,052,917.00
Funds Obligated to Date: FY 2018 = $1,052,917.00
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
496 W 12th Ave
Columbus
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: 01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1097, 1389, 8811, 9117
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

In the oceans, microbial life sits at the base of the food chain, but microbes also control the flow of nutrients and energy. While our knowledge of microbial impacts on the oceans is rapidly advancing, we remain far behind in studying the impact of viruses. Decades of experiments and global surveys that have focused on common ocean viruses (double-stranded DNA viruses) suggest that they kill many cells, change the genes that cells encode in their genomes, and reprogram how cells function during infection. This project seeks to create a metabolic map of the global oceans and quantify which of these microbial processes common viruses manipulate. Further, this project will expand to other types of viruses (RNA viruses) that are less well studied, as well as advance our knowledge of both DNA and RNA viruses with respect to global patterns and distributions to assess viral activity. Such analyses are critical to better understand how viruses of all types alter microbial processes and thereby drive nutrient cycling in the oceans. Beyond the science, this project will train two postdocs, a graduate student and five undergraduate students, as well as conduct outreach through Columbus-area seminars and lecture series and provide a training workshop for researchers in each years 1 and 3.

Microbial metabolisms alter nutrients and energy flow in ways that impact global ocean biogeochemistry, but associated viruses modulate these metabolic impacts through mortality, horizontal gene transfer and metabolic reprogramming. The latter impact is particularly understudied due to being a largely manual process, though early data hints that it likely impacts photosynthesis, central carbon metabolism, and nitrogen and sulfur cycling. Further, though eukaryotes are likely most commonly infected by RNA viruses and RNA viruses are thought to represent about half of viral particles in seawater, very little information on RNA virus diversity or ecology exists. Finally, particles are not the ?active? form of viruses, which begs for the development of new approaches to assess activity using the newly-available reference genomes against expression (e.g., metatranscriptomic) datasets. This project seeks to leverage extensive organismal, physical, and chemical datasets from the global Tara Oceans expedition to (i) advance from surveying dsDNA viral biodiversity towards inferring their metabolic impacts and active infection ecology, and (ii) build a parallel RNA virus biodiversity inventory from which to establish foundational ecological understanding of drivers and community structure. Scientifically, these efforts will evaluate more than a dozen hypotheses and establish countless more hypotheses about viral roles in marine microbial ecology and biogeochemistry. The project will train two postdocs, a graduate student and five undergraduate students, some through engagement with international Tara Oceans Consortium meetings, as well as provide public outreach through classroom and seminar visits at a Columbus area school (~240 students), a local chapter of the MIT Alumni club, an OSU Center for RNA Biology ?Science Sundays? lecture series, and seminars and interactive activities with Canada?s indigenous people. A viromics training workshop will be held in each years 1 and 3 to maximize research community involvement and engagement.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

Note:  When clicking on a Digital Object Identifier (DOI) number, you will be taken to an external site maintained by the publisher. Some full text articles may not yet be available without a charge during the embargo (administrative interval).

Some links on this page may take you to non-federal websites. Their policies may differ from this site.

(Showing: 1 - 10 of 19)
Gazitúa, M. Consuelo and Vik, Dean R. and Roux, Simon and Gregory, Ann C. and Bolduc, Benjamin and Widner, Brittany and Mulholland, Margaret R. and Hallam, Steven J. and Ulloa, Osvaldo and Sullivan, Matthew B. "Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters" The ISME Journal , v.15 , 2020 https://doi.org/10.1038/s41396-020-00825-6 Citation Details
Vik, Dean and Gazitúa, Maria Consuelo and Sun, Christine L. and Zayed, Ahmed A. and Aldunate, Montserrat and Mulholland, Margaret R. and Ulloa, Osvaldo and Sullivan, Matthew B. "Genome?resolved viral ecology in a marine oxygen minimum zone" Environmental Microbiology , v.23 , 2020 https://doi.org/10.1111/1462-2920.15313 Citation Details
Moran, Mary Ann and Kujawinski, Elizabeth B. and Schroer, William F. and Amin, Shady A. and Bates, Nicholas R. and Bertrand, Erin M. and Braakman, Rogier and Brown, C. Titus and Covert, Markus W. and Doney, Scott C. and Dyhrman, Sonya T. and Edison, Arthu "Microbial metabolites in the marine carbon cycle" Nature Microbiology , v.7 , 2022 https://doi.org/10.1038/s41564-022-01090-3 Citation Details
Howard-Varona, Cristina and Roux, Simon and Bowen, Benjamin P. and Silva, Leslie P. and Lau, Rebecca and Schwenck, Sarah M. and Schwartz, Samuel and Woyke, Tanja and Northen, Trent and Sullivan, Matthew B. and Floge, Sheri A. "Protist impacts on marine cyanovirocell metabolism" ISME Communications , v.2 , 2022 https://doi.org/10.1038/s43705-022-00169-6 Citation Details
Richter, Daniel J and Watteaux, Romain and Vannier, Thomas and Leconte, Jade and Frémont, Paul and Reygondeau, Gabriel and Maillet, Nicolas and Henry, Nicolas and Benoit, Gaëtan and Da Silva, Ophélie and Delmont, Tom O and Fernàndez-Guerra, Antonio and Su "Genomic evidence for global ocean plankton biogeography shaped by large-scale current systems" eLife , v.11 , 2022 https://doi.org/10.7554/eLife.78129 Citation Details
Paoli, Lucas and Ruscheweyh, Hans-Joachim and Forneris, Clarissa C. and Hubrich, Florian and Kautsar, Satria and Bhushan, Agneya and Lotti, Alessandro and Clayssen, Quentin and Salazar, Guillem and Milanese, Alessio and Carlström, Charlotte I. and Papadop "Biosynthetic potential of the global ocean microbiome" Nature , v.607 , 2022 https://doi.org/10.1038/s41586-022-04862-3 Citation Details
Dominguez-Huerta, Guillermo and Zayed, Ahmed A. and Wainaina, James M. and Guo, Jiarong and Tian, Funing and Pratama, Akbar Adjie and Bolduc, Benjamin and Mohssen, Mohamed and Zablocki, Olivier and Pelletier, Eric and Delage, Erwan and Alberti, Adriana an "Diversity and ecological footprint of Global Ocean RNA viruses" Science , v.376 , 2022 https://doi.org/10.1126/science.abn6358 Citation Details
Zayed, Ahmed A. and Wainaina, James M. and Dominguez-Huerta, Guillermo and Pelletier, Eric and Guo, Jiarong and Mohssen, Mohamed and Tian, Funing and Pratama, Akbar Adjie and Bolduc, Benjamin and Zablocki, Olivier and Cronin, Dylan and Solden, Lindsey and "Cryptic and abundant marine viruses at the evolutionary origins of Earth?s RNA virome" Science , v.376 , 2022 https://doi.org/10.1126/science.abm5847 Citation Details
Salazar, Guillem and Paoli, Lucas and Alberti, Adriana and Huerta-Cepas, Jaime and Ruscheweyh, Hans-Joachim and Cuenca, Miguelangel and Field, Christopher M. and Coelho, Luis Pedro and Cruaud, Corinne and Engelen, Stefan and Gregory, Ann C. and Labadie, K "Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome" Cell , v.179 , 2019 10.1016/j.cell.2019.10.014 Citation Details
Schmidt, Jörn O. and Bograd, Steven J. and Arrizabalaga, Haritz and Azevedo, José L. and Barbeaux, Steven J. and Barth, John A. and Boyer, Tim and Brodie, Stephanie and Cárdenas, Juan José and Cross, Scott and Druon, Jean-Noël and Fransson, Agneta and Har "Future Ocean Observations to Connect Climate, Fisheries and Marine Ecosystems" Frontiers in Marine Science , v.6 , 2019 10.3389/fmars.2019.00550 Citation Details
Ibarbalz, Federico M. and Henry, Nicolas and Brandão, Manoela C. and Martini, Séverine and Busseni, Greta and Byrne, Hannah and Coelho, Luis Pedro and Endo, Hisashi and Gasol, Josep M. and Gregory, Ann C. and Mahé, Frédéric and Rigonato, Janaina and Royo- "Global Trends in Marine Plankton Diversity across Kingdoms of Life" Cell , v.179 , 2019 10.1016/j.cell.2019.10.008 Citation Details
(Showing: 1 - 10 of 19)

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.

Throughout the global oceans, microscopic organisms such as protists, bacteria, and viruses - collectively called plankton - carry out essential ecosystem functions. These plankton serve as the foundation of marine food webs and they control biogeochemical cycles that fuel the planet. Plankton also acts as a biological carbon pump that dictates what to do with human-released carbon dioxide that the ocean absorbs from the atmosphere. Over a decade ago, an international project - the Tara Oceans Expedition - was launched to systematically sample, catalog, and study the plankton throughout the world?s oceans. Through NSF funding, we previously discovered over 200,000 ?species? of bacteria-infecting DNA viruses and found that they impact the ocean biological carbon pump, and also contained ?exotic? metabolism genes in their genomes such as photosynthesis and nitrogen metabolism genes. If viruses ?stole? these genes and repurposed them for infection, is this another way viruses impact the plankton and overall biogeochemical cycles? How many such metabolism genes have viruses stolen and do they follow any ecological patterns?

Our current NSF-funded project builds on this prior work in two ways. First, we wanted to dive deeper into the ecology and impact of these virus-encoded metabolism genes, to establish a baseline understanding of how viruses might directly impact their host metabolism, and how these are distributed throughout the global oceans. We found that about 1 in 10 marine viruses carries at least one such metabolic gene and developed a global catalog for the range of metabolisms viruses could directly impact. We also found that the abundance of these metabolic functions encoded varied by ocean region and depth. Such data provide foundational ecological information that will be used in future work to parameterize models of how the oceans work.

Second, this current project opened up a window into a previously near-completely neglected fraction of the viruses in the oceans - RNA viruses. To do this, we developed a novel detection pipeline, implemented a classification framework, and unraveled the biogeographical patterns of RNA viruses on a global scale that resulted in two papers published in Science. Specifically, our novel detection methods identified 5,504 RNA virus ?species?, and >99% were new species that spanned all 5 known RNA virus phyla (high-level classifications), but also revealed 5 entirely new phyla and 11 new classes.  With all these new RNA viruses now ?visible? to us, we next studied their ecological patterns, drivers, and community structure, and found that they were organized around four ecological zones, and had diversity correlates with latitude, depth, and environmental variables like temperature. For example, nutrients were a strong predictor of RNA virus diversity, while depth correlated with decreased diversity. When we used machine learning and ecosystem modeling approaches to assess RNA virus roles in the ocean biological carbon pump, we see that their abundances were strongly predictive, and identified 11 specific RNA viruses that were most significant for these predictions (great targets for follow-on work). Just like with DNA viruses, we also saw that RNA viruses have stolen metabolic genes hinting at specific ways they too could be critical members of carbon flux in the oceans.

Overall, the data resources, discoveries, and analytical tools that enabled them that resulted from this award will have broad impacts across several fields including virus ecology, marine microbiology, biological oceanography, microbiome science, epidemiology, as well as human and veterinary medicine. For example, our improved virus-encoded metabolic gene catalogs and RNA virus catalogs, and associated new paradigms, will be critical for oceanographic modelers, while our new RNA virus identification and classification pipelines will have impacts well outside the oceans.

 


Last Modified: 12/02/2022
Modified by: Matthew Sullivan

Please report errors in award information by writing to: awardsearch@nsf.gov.

Print this page

Back to Top of page