Award Abstract # 1756884
Collaborative Research: Iron Bioavailability in High-CO2 Oceans: New Perspectives on Iron Acquisition Mechanisms in Diatoms

NSF Org: OCE
Division Of Ocean Sciences
Recipient: J. CRAIG VENTER INSTITUTE, INC.
Initial Amendment Date: February 6, 2018
Latest Amendment Date: February 6, 2018
Award Number: 1756884
Award Instrument: Standard Grant
Program Manager: Michael Sieracki
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: February 15, 2018
End Date: January 31, 2022 (Estimated)
Total Intended Award Amount: $878,652.00
Total Awarded Amount to Date: $878,652.00
Funds Obligated to Date: FY 2018 = $878,652.00
History of Investigator:
  • Andrew Allen (Principal Investigator)
    aallen@ucsd.edu
Recipient Sponsored Research Office: J. Craig Venter Institute, Inc.
4120 CAPRICORN LN
LA JOLLA
CA  US  92037-3498
(858)200-1864
Sponsor Congressional District: 50
Primary Place of Performance: J. Craig Venter Institute
4120 Capricorn Lane
La Jolla
CA  US  92037-3498
Primary Place of Performance
Congressional District:
50
Unique Entity Identifier (UEI): FL8UNYTG72D1
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1382, 1389, 9117
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Collaborative Research: Iron Bioavailability in High-CO2 Oceans: New Perspectives on Iron Acquisition Mechanisms in Diatoms

Iron is critically needed for growth of all marine phytoplankton, the microscopic plants at the base of the ocean food chain. Consequently, lack of iron in large regions of the global ocean limits phytoplankton growth and commercial fisheries. Ocean acidification (OA) is the ongoing decrease in seawater pH due to the ocean absorbing carbon dioxide from the atmosphere. OA is predicted to affect seawater chemistry by reducing the concentration of carbonate ions. Carbonate ions are required for phytoplankton to take up iron from their environment, which suggests that OA might inhibit iron nutrition. Further complicating the scenario, pH changes affect iron chemistry in seawater, such that OA is predicted to shift the relative abundance of various forms of iron. But despite these expectations, little is known about how the changes in ocean chemistry due to OA will impact the availability of iron to phytoplankton. Changes in phytoplankton iron uptake and associated growth rates would likely have large effects on how the ocean captures atmospheric carbon dioxide (CO2). This has important consequences for ecosystem productivity and for global cycles of critical chemical elements, such as carbon and nitrogen, and their chemistry. This project aims to help us understand how shifts in seawater pH and the chemistry of dissolved inorganic carbon will affect both iron uptake rates and iron acquisition strategies in the laboratory and in natural communities. This project also includes development of educational outreach activities which target primary school students in the areas of microbiology, biogeochemical cycles and current global change topics. These science outreach activities benefit from collaborations with the following San Diego-based organizations: the League of Extraordinary Scientists and Engineers (LXS), The Birch Aquarium at Scripps (BAS), and The Ocean Discovery Institute (ODI).

This project seeks to understand the differential sensitivity of diatom iron acquisition strategies to changes in seawater pH and carbonate chemistry. Ultimately a more thorough and detailed mechanistic understanding of diatom iron uptake pathways will facilitate a much-improved ability to forecast the impact of anticipated changes in ocean pH and inorganic carbon chemistry on rates of iron uptake by diatoms. This critical biogeochemical issue is addressed through trace metal clean manipulation experiments incorporating state-of-the-art analytical methodology to probe phytoplankton cellular physiology and biogeochemistry in laboratory cultures and natural communities. In the first year, laboratory experiments with a model pennate diatom leverage a collection of targeted knockout transgenic lines to evaluate the substrate specificity and relative importance of distinct iron assimilation pathways under a range of pCO2 and iron availability conditions. Additionally, quantitation of mRNA and proteins for key diatom iron assimilation pathways in natural communities in the Southern California Current further clarify the relative importance and sensitivity of distinct iron assimilation pathways in relation to pCO2 and iron availability. In year two a Lagrangian study of iron uptake rates and associated mRNA and protein abundance is performed on upwelled high pCO2 water over the course of offshore advection. Additionally, the investigators are conducting mesocosm experiments using naturally elevated high pCO2 seawater as well as laboratory experiments on multiplex knockout lines. Year three is dedicated to data analyses and overall project synthesis. Overall aims of the research activities include, 1) development and validation of a refined conceptual model of iron uptake in key marine phytoplankton and subsequent utilization of the model to characterize the sensitivity of distinct iron uptake pathways to the effects of ocean acidification, and 2) determination of the effects of acidification on iron uptake, and quantification of the relative contribution of distinct iron acquisition pathways in high pCO2 phytoplankton communities.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 14)
Breier, John A. and Jakuba, Michael V. and Saito, Mak A. and Dick, Gregory J. and Grim, Sharon L. and Chan, Eric W. and McIlvin, Matthew R. and Moran, Dawn M. and Alanis, Brianna A. and Allen, Andrew E. and Dupont, Chris L. and Johnson, Rod "Revealing ocean-scale biochemical structure with a deep-diving vertical profiling autonomous vehicle" Science Robotics , v.5 , 2020 https://doi.org/10.1126/scirobotics.abc7104 Citation Details
Coale, Tyler H. and Moosburner, Mark and Horák, Ale and Oborník, Miroslav and Barbeau, Katherine A. and Allen, Andrew E. "Reduction-dependent siderophore assimilation in a model pennate diatom" Proceedings of the National Academy of Sciences , v.116 , 2019 10.1073/pnas.1907234116 Citation Details
Cohen, Natalie R. and McIlvin, Matthew R. and Moran, Dawn M. and Held, Noelle A. and Saunders, Jaclyn K. and Hawco, Nicholas J. and Brosnahan, Michael and DiTullio, Giacomo R. and Lamborg, Carl and McCrow, John P. and Dupont, Chris L. and Allen, Andrew E. "Dinoflagellates alter their carbon and nutrient metabolic strategies across environmental gradients in the central Pacific Ocean" Nature Microbiology , 2021 https://doi.org/10.1038/s41564-020-00814-7 Citation Details
Diner, Rachel E. and Kaul, Drishti and Rabines, Ariel and Zheng, Hong and Steele, Joshua A. and Griffith, John F. and Allen, Andrew E. and Seyler, Lauren Marie "Pathogenic Vibrio Species Are Associated with Distinct Environmental Niches and Planktonic Taxa in Southern California (USA) Aquatic Microbiomes" mSystems , v.6 , 2021 https://doi.org/10.1128/mSystems.00571-21 Citation Details
Jabre, Loay J. and Allen, Andrew E. and McCain, J. Scott and McCrow, John P. and Tenenbaum, Nancy and Spackeen, Jenna L. and Sipler, Rachel E. and Green, Beverley R. and Bronk, Deborah A. and Hutchins, David A. and Bertrand, Erin M. "Molecular underpinnings and biogeochemical consequences of enhanced diatom growth in a warming Southern Ocean" Proceedings of the National Academy of Sciences , v.118 , 2021 https://doi.org/10.1073/pnas.2107238118 Citation Details
Kolody, B. C. and McCrow, J. P. and Allen, L. Zeigler and Aylward, F. O. and Fontanez, K. M. and Moustafa, A. and Moniruzzaman, M. and Chavez, F. P. and Scholin, C. A. and Allen, E. E. and Worden, A. Z. and Delong, E. F. and Allen, A. E. "Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection" The ISME Journal , v.13 , 2019 https://doi.org/10.1038/s41396-019-0472-2 Citation Details
Kranzler, Chana F. and Krause, Jeffrey W. and Brzezinski, Mark A. and Edwards, Bethanie R. and Biggs, William P. and Maniscalco, Michael P. and McCrow, John A. and Van Mooy, Benjamin D. and Bidle, Kay E. and Allen, Andrew and Thamatrakoln, Kimberlee "Silicon limitation facilitates virus infection and mortality of marine diatoms" Nature Microbiology , v.4 , 2019 10.1038/s41564-019-0502-x Citation Details
Krause, Jeffrey W. and Brzezinski, Mark A. and Largier, John L. and McNair, Heather M. and Maniscalco, Michael and Bidle, Kay D. and Allen, Andrew E. and Thamatrakoln, Kimberlee "The interaction of physical and biological factors drives phytoplankton spatial distribution in the northern California Current" Limnology and Oceanography , v.65 , 2020 https://doi.org/10.1002/lno.11431 Citation Details
McCain, J. Scott and Tagliabue, Alessandro and Susko, Edward and Achterberg, Eric P. and Allen, Andrew E. and Bertrand, Erin M. "Cellular costs underpin micronutrient limitation in phytoplankton" Science Advances , v.7 , 2021 https://doi.org/10.1126/sciadv.abg6501 Citation Details
Moosburner, Mark Andrew and Gholami, Pardis K. and McCarthy, James A. and Tan, Maxine E. and Bielinski, Vincent and Allen, Andrew "Multiplexed Knockouts in the Model Diatom Phaeodactylum by Episomal Delivery of a Selectable Cas9" Frontiers in Microbiology , v.11 , 2020 10.3389/fmicb.2020.00005 Citation Details
Stephens, Brandon M. and Wankel, Scott D. and Beman, J. Michael and Rabines, Ariel J. and Allen, Andrew E. and Aluwihare, Lihini I. "Euphotic zone nitrification in the California Current Ecosystem" Limnology and Oceanography , v.65 , 2019 https://doi.org/10.1002/lno.11348 Citation Details
(Showing: 1 - 10 of 14)

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.

Iron Bioavailability in High-CO2 Oceans: New Perspectives on Iron Acquisition Mechanisms in Diatoms

 

Intellectual Merit: Coastal upwelling regions are among the most biologically productive ecosystems in the ocean but may be threatened by amplified ocean acidification from rising atmospheric CO2. Also, it has become increasingly clear that iron availability plays a major role in regulating the fate of upwelled nitrate (NO3-) and determining the size structure and community composition of phytoplankton assemblages in open-ocean and coastal upwelling regions. However, the molecular mechanisms that govern inorganic iron uptake in ocean phytoplankton are believed to be contingent on carbonate ion concentrations. Therefore, increased acidification is hypothesized to reduce iron bioavailability for marine phytoplankton thereby expanding iron limitation and impacting primary production. Field and laboratory studies conducted through this project showed, from community to molecular levels, that iron-stressed phytoplankton in an upwelling region exhibit resistance to short-term acidification. Molecular-level responses, from studies conducted at sea, showed that, although variable. resistance to acidification-driven changes in iron bioavailability is facilitated by iron uptake pathways that are less hindered by acidification and other cellular strategies that reduce cellular iron demand. These mechanisms, however, may only confer resistance over short time periods, and chronic long-term exposure may result in further iron stress. These field studies confirm that, as ocean acidification reduces carbonate concentrations, inorganic iron uptake may be discouraged in favor of carbonate-independent uptake.  Findings from laboratory studies uncovered the biochemical function and evolution of the proteins responsible for diatom acquisition of iron from bacterial siderophores; a mechanism that does not have a carbonate requirement but requires a bacteria-diatom interaction. We demonstrated that the diatom siderophore acquisition system is composed of a hydroxamate siderophore receptor protein of bacterial origin and a NADPH oxidase type ferric reductase of eukaryotic origin. Additionally, using an optimized protocol for subcellular proteomics we further characterized the proteins and processes that occur downstream of diatom iron binding at the cell surface. Based on these results, coupled to additional in vivo and biochemical experiments and evolutionary analyses, we derived a new view of key endosomal processes and biochemical transformations that mediate subsequent intracellular allocation of internalized Fe(III). Finally, using all of our data, we obtained a new comprehensive conceptual overview for iron-trafficking, from the cell surface to the chloroplast.

 

Broader Impacts:  A curricular module related to marine microbes and the ocean carbon cycle in the marine environment was developed through the San Diego- based League of Extraordinary Scientists and Engineers http://science-ing.org (LXS). The LXS mission is engaging young people from underserved communities to inspire them to become part of the next generation of scientific and environmental leaders. During the award period, LXS brought science to over 4,500 public elementary school classrooms.


Last Modified: 02/08/2022
Modified by: Andrew E Allen

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