Award Abstract # 1849926
Collaborative Research: Elucidating algal host-virus dynamics in different nutrient regimes - mechanistic interactions and biogeochemical impact

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF TENNESSEE
Initial Amendment Date: September 4, 2018
Latest Amendment Date: September 4, 2018
Award Number: 1849926
Award Instrument: Standard Grant
Program Manager: Michael Sieracki
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: June 1, 2018
End Date: September 30, 2019 (Estimated)
Total Intended Award Amount: $55,642.00
Total Awarded Amount to Date: $55,642.00
Funds Obligated to Date: FY 2015 = $55,642.00
History of Investigator:
  • David Talmy (Principal Investigator)
    dtalmy@utk.edu
Recipient Sponsored Research Office: University of Tennessee Knoxville
201 ANDY HOLT TOWER
KNOXVILLE
TN  US  37996-0001
(865)974-3466
Sponsor Congressional District: 02
Primary Place of Performance: University of Tennessee Knoxville
1 Circle Park
Knoxville
TN  US  37996-0003
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): FN2YCS2YAUW3
Parent UEI: LXG4F9K8YZK5
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001516DB 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

Marine phytoplankton, photosynthetic microscopic organisms that float with the oceans currents, account for ~50% of the Earth's primary productivity. When there are sufficient nutrients and light to sustain their growth, phytoplankton thrive and produce large-scale blooms in the world oceans that can be seen from Earth-observing satellites. Coccolithophores are arguably one of the most dominant and globally distributed phytoplankton. Their dual ability to produce calcium carbonate cell walls and to use carbon dioxide for photosynthesis make them a key component of the oceanic carbon cycle and marine ecosystems. As such, water column processes that impact the fate of this cellular carbon are of critical importance. Emiliania huxleyi is a globally widespread, cosmopolitan coccolithophore that forms blooms in all but the polar oceans. These blooms are routinely terminated by virus infection (Coccolithoviruses), which results in cell death and the release of organic matter into the upper ocean. At the same time, infection triggers the production and release of a sticky mucus-like gel which serves to aggregate free floating cells (and even viruses) into larger particles that have very high sinking rates into the deep ocean. Hence, viruses play multifaceted roles in determining whether phytoplankton carbon sinks to the deep ocean and is sequestered away from the atmosphere or is recycled in the upper ocean free to exchange with the atmosphere. Ultimately, factors that impact the interactions between phytoplankton cells and viruses are likely to affect the direction of carbon flow in the oceans. This project uses a well-characterized, laboratory-based coccolithophore-virus system (E. huxleyi and Coccolithoviruses) to elucidate the basic mechanisms that underlie host-virus interactions at the levels of adsorption, replication and production. Proposed work will manipulate nutrient supply to understand its impact on mechanisms of infection and to better interpret population changes in different oceanic regimes. A key tenet is to investigate the role of mucus-like gels and calcium carbonate cell walls, both of which are produced under nutrient stress, as important first order drivers in host-virus interactions. Experimental work will be integrated into mathematical models as a tool to extrapolate our findings and postulate how, to first order, viruses control the fate of phytoplankton populations in the ocean. Research concepts and findings will be relayed to broader audiences by developing an online educational software tool and web app (via the Rutgers University Mobile App Development group) that focuses on the use of mathematical modeling in marine science. It will be designed to meet national requirements for the Next Generation Science Standards (NGSS) for 15-16 year olds. Students will learn about patterns of ocean productivity, articulate how and why ocean ecosystems are sensitive to environmental change, and understand the role of viruses in ecosystem structure. To ensure large-scale distribution of the app, with a particular aim to reach underrepresented students and to address the NGSS, Rutgers will host workshops to familiarize the teachers with the science, the scientists, and effective use of the app and associated lessons. The investigators will work with external evaluators to assess the effectiveness of these activities and deliverables. Research activities will also be communicated to the general public by interactions with the 'Liquid Living' display at the San Francisco Exploratorium and the annual 'Nautical Night' at the MIT museum in Boston, MA.


Phytoplankton are the basis of marine food webs and are responsible for approximately half of global net primary production. As highly abundant infectious entities in the oceans, marine viruses can cause the demise of phytoplankton blooms and drive the release of dissolved and particulate organic matter (DOM and POM), which stimulates microbial activity, facilitates bacterial re-mineralization, enhances nutrient recycling and respiration, as well as short-circuits carbon transport to higher trophic levels. At the same time, enhanced production and release of "sticky" colloidal cellular components, such as transparent exopolymer particles (TEP), during viral lysis can cause particle aggregation and enhance carbon export. As yet, the dynamics of phytoplankton infection by viruses and the balance between these diametrically opposed ecosystem pathways has not been fully characterized under different physicochemical conditions. An enhanced mechanistic and quantitative understanding of host-virus interactions can critically inform and constrain ecosystem models and allow researchers to ascertain and quantify its ecological and biogeochemical impacts on large spatial scales. This collaborative project aims to bridge existing gaps in our mechanistic and quantitative understanding of viruses as agents of phytoplankton mortality and their impact on biogeochemical processes. The ability of ecosystem models to predict carbon flow in marine systems is limited, in part, by a lack of appropriate information regarding the nutrient sensitivity of fundamental infection parameters: viral adsorption rates onto/into hosts, virus replication efficiency and latent period, and the production of infectious viruses and their excretion into the surrounding medium. Using lab-based experiments with a coccolithophore host-virus model system, as well as extensive datasets from virus infected natural coccolithophore blooms in the North Atlantic, this project aims to elucidate the impact of nutrient limitation and host cell fitness on virus infection and to what degree the dependence of viral infection on nutrient supply impacts large scale biogeochemistry and biogeography of a globally significant phytoplankton species. Our interdisciplinary approach combines grounded molecular- and flow cytometry-based diagnostic techniques, with the development of a mathematical model of infection, to understand the primary mechanisms underlying observed host-virus dynamics. We will embed the mathematical model of infection dynamics into a global ecosystem model, so we may understand the ecological impact of phytoplankton infection by viruses, and its dependence on nutrient supply, on large spatial scales.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Nissimov, J.I., Talmy, D., Haramaty, L., Fredricks, H., Zelzion, U., Eren, M., Gardella, R., Laber, C., More, K.D., Bhattacharya, D., Follows, M.J., Coolen, M.J.L., Van Mooy, B.A.S., Bidle, K.D. "Biochemical diversity of sphingolipid biosynthesis as a driver of algal-virus competitive ecology" Environmental Microbiology , v.21 , 2019 , p.2182 https://doi.org/10.1111/1462-2920.14633
Talmy, D., Beckett, S.J., Taniguchi, D.A.A., Weitz, J., Follows, M.J. "An empirical model of carbon transfer through marine viruses and microzooplankton grazers." Environmental Microbiology , v.21 , 2019 , p.2171 https://doi.org/10.1111/1462-2920.14626
Talmy, D., Beckett, S.J., Taniguchi, D.A.A., Weitz, J., Follows, M.J. "Contrasting controls on microzooplankton grazing and viral infection of microbial prey." Frontiers in Marine Science , v.6 , 2019 10.3389/fmars.2019.00182
Thamatrakoln, K., Talmy, D., Haramaty, L., Maniscalo, C., Latham, J., Knowles, B., Natale, F., Coolen, M.J.L., Follows, M.J., Bidle, K.D., "Light regulation of coccolithophore host-virus interactions." New Phytologist , 2018 10.1111/nph.15459

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.

Marine phytoplankton are responsible for approximately 50% of global carbon fixation. Viral infection of marine phytoplankton influences marine ecosystems by controlling community composition, and directing the flow of organic matter and energy. Understanding the diverse and complex roles of viruses in marine systems requires the development of mathematical models which integrate and synthesize the interacting physical, biological, and chemical mechanisms that influence how algal host-virus interactions are coupled with system function. This project focused on the development of ecosystem models to assess the effects of marine viruses on marine planktonic ecosystems on large spatial scales. 

A major goal of theoretical work conducted at the University of Tennessee, Knoxville, was to interpret data gathered during field expeditions and laboratory experiments conducted by an experimental group led by Professor Kay Bidle at Rutgers University. The Bidle group combined molecular and flow-cytometry techniques to identify how calcifying marine phytoplankton, the coccolithophore Emiliania huxleyi, were sensitive to infection by EhV viruses. The Bidle group used genetic and lipid markers to detect specific signatures of viral infection along transects in the North Atlantic. An article reporting these findings, with a complementary ecosystem model investigation of mechanisms controlling observed community composition, was published in the journal Environmental Microbiology (Nissimov et al. 2019).

In addition to the coccolithophores, marine viruses have been reported to infect nearly all major functional groups of phytoplankton, as well as heterotrophic bacteria and some microzooplankton. Understanding the effects of viruses on the dynamics of coccolithophores therefore requires understanding of how viruses influence the dynamics of competing groups, such as diatoms and cyanobacteria. A focus of this project was to combine biophysical principles with laboratory and environmental data to develop a general, trait-based framework to quantitatively describe and constrain viral infection, and how this contrasts with other major contributors to microbial mortality. Research synthesizing diverse controls on microbial predator-prey dynamics was reported in several journal publications (Record et al. 2016; Talmy et al. 2019a;b).

Viral infection of microbial hosts takes place over large spatial contexts which encompass large shifts in light, nutrient, and temperature conditions. Understanding the global-scale impacts of viruses on marine ecosystems requires understanding how viral infection is sensitive to changes in abiotic conditions. A major focus of this work was to use mathematical models to characterize shifts in host-virus population dynamics in response to changes in light, temperature, and nutrients. A study exploring sensitivity of E. huxleyi-EhV infection dynamics to a range of light intensities was reported in the journal the New Phytologist (Thamatrakoln et al. 2019). Complementary investigations exploring sensitivity of infection to changes in nutrient availability and temperature, in a diverse set of microbial host-virus systems, are ongoing and manuscripts reporting the findings will be submitted for publication in the near future.

This project has provided a basis for understanding the impacts of viruses within microbial ecosystems at large spatial scales. The major advancement of this project therefore lies in the foundation of a framework to enable assessment of how viral activity impacts the Earth and climate system. The successful combination of dynamic models, laboratory data, and environmental ecosystem research has elucidated key mechanisms driving host-virus dynamics in diverse marine systems, and provides a model for synthesizing diverse predator-prey interactions and their coupling with global carbon dynamics and biogeochemistry.

Nissimov, J. I., D. Talmy, L. Haramaty, H. Fredricks, E. Zelzion, B. Knowles, M. Eren, R. Vandzura, C. P. Laber, B. M. Schieler, C. T. Johns, K. More, M. J. L. Coolen, M. J. Follows, D. Bhattacharya, B. A. S. Van Mooy, and K. D. Bidle. 2019. Biochemical diversity of glycosphingolipid biosynthesis as a driver of Coccolithovirus competitive ecology. Environ. Microbiol. 21: 2182?2197.

Record, N. R., D. Talmy, and S. Vage. 2016. Quantifying tradeoffs for marine viruses. Front. Mar. Sci. 3: 1?27.

Talmy, D., S. J. Beckett, D. A. A. Taniguchi, C. P. D. Brussaard, J. S. Weitz, and M. J. Follows. 2019a. An empirical model of carbon flow through marine viruses and microzooplankton grazers. Environ. Microbiol. 21: 2171?2181.

Talmy, D., S. J. Beckett, A. B. Zhang, D. A. A. Taniguchi, J. S. Weitz, and M. J. Follows. 2019b. Contrasting controls on microzooplankton grazing and viral infection of microbial prey. Front. Mar. Sci. 6: 1?12.

Thamatrakoln, K., D. Talmy, L. Haramaty, C. Maniscalco, J. R. Latham, B. Knowles, F. Natale, M. J. L. Coolen, M. J. Follows, and K. D. Bidle. 2019. Light regulation of coccolithophore host?virus interactions. New Phytol. 221: 1289?1302.

 


Last Modified: 12/30/2019
Modified by: David Talmy

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