Award Abstract # 1434916
Photoheterotrophy in unicellular cyanobacteria: ecological drivers and significance for marine biogeochemistry

NSF Org: OCE
Division Of Ocean Sciences
Recipient: THE TRUSTEES OF COLUMBIA UNIVERSITY IN THE CITY OF NEW YORK
Initial Amendment Date: June 16, 2014
Latest Amendment Date: June 16, 2014
Award Number: 1434916
Award Instrument: Standard Grant
Program Manager: Michael Sieracki
OCE
 Division Of Ocean Sciences
GEO
 Directorate For Geosciences
Start Date: September 1, 2014
End Date: August 31, 2018 (Estimated)
Total Intended Award Amount: $334,185.00
Total Awarded Amount to Date: $334,185.00
Funds Obligated to Date: FY 2014 = $334,185.00
History of Investigator:
  • Solange Duhamel (Principal Investigator)
    duhamel@email.arizona.edu
Recipient Sponsored Research Office: Columbia University
615 W 131ST ST
NEW YORK
NY  US  10027-7922
(212)854-6851
Sponsor Congressional District: 13
Primary Place of Performance: Lamont-Doherty Earth Observatory of Columbia University
61 Route 9W
Palisades
NY  US  10964-1707
Primary Place of Performance
Congressional District:
17
Unique Entity Identifier (UEI): F4N1QNPB95M4
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001415DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1389, 8811
Program Element Code(s): 1650
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Title: Photoheterotrophy in Unicellular Cyanobacteria: Ecological Drivers and Significance for Marine Biogeochemistry

Unicellular cyanobacteria are major contributors to primary production and carbon export in the open ocean. They also play an important role in the control of nutrient availability. The ability of these microbes to harvest light energy benefits a range of physiological functions, but the effect of light on their metabolism (other than for photosynthesis) is poorly known and controversial. This project will investigate the role of light in uptake of organic substrates (carbon and nutrients) by unicellular cyanobacteria and elucidate the importance of photoheterotrophy. The ability of these organisms to assimilate organic compounds and its modulation by light and nutrients will provide additional hints about the ecological success of unicellular cyanobacteria in the ocean. The proposed work will involve field experiments in the southwest Pacific Ocean, complemented by laboratory experiments in controlled cultures of ecologically relevant cyanobacteria. The study will employ innovative methods, including single cell assays and molecular tools that target individual cyanobacteria and evaluate their response to light for the assimilation of organic substrates. This research project will lead to an increased understanding of the microbial adaptations to light and nutrient gradients and the role these adaptations play in elemental cycling in oceanic habitats. This project will support an early career female investigator. Both undergraduate students and local high school students will be trained in research techniques and mentored by the investigator. Findings resulting from this project will be communicated to scientists through open-access publications. A video documenting the scientific cruise and summarizing the major discoveries of the proposed research will be produced and be widely accessible to the public. These activities will thus reach a broad audience including a significant fraction of underrepresented groups.


Unicellular cyanobacteria inhabit the surface ocean (generally <150 m deep), and use solar energy to compete for a limited supply of available nutrients. Therefore, they are expected to utilize light energy not only for photosynthesis but also to enhance their metabolism of dissolved organic compounds. Yet, the role of light in the uptake of organic compounds (both carbon and nutrients) and the importance of photoheterotrophy are still poorly understood. This proposal seeks to investigate the ecological drivers and significance of photoheterotrophy in the unicellular cyanobacteria Prochlorococcus and Synechococcus, the most abundant groups of primary producers in the ocean, and Crocosphaera an important nitrogen fixing organism. This proposal argues that adaptations to specific light regimes must shape spatiotemporal partitioning of resources among microbial groups in the ocean. Field experiments along a west-east transect in the southwest Pacific Ocean will cover a range of nutrient conditions and cyanobacterial abundances. Radioactive substrate incubations combined with flow cytometry cell sorting and microautoradiography paired to catalyzed reporter deposition fluorescence in situ hybridization (MICRO-CARD-FISH) will allow the separation of unicellular cyanobacteria from non-pigmented bacterioplankton and evaluation of their response to light for the uptake of different organic substrates. These experiments will be complemented by laboratory tests in controlled cultures of axenic strains representative of different ecologically relevant functional groups of cyanobacteria. Lastly, the capacity of the important nitrogen fixer Crocosphaera watsonii to feed on glucose will be tested, taking advantage of the sequenced genome of the representative strain WH8501 in targeting the expression of genes involved in glucose metabolism in situ.

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 20)
Benavides M., Berthelot H., Raimbault P., Duhamel S., S. Bonnet. "Dissolved organic matter uptake by Trichodesmium in the Southwest Pacific." Nature Scientific Reports , v.7 , 2017 , p.41315 10.1038/srep41315
Benavides M., Shoemaker K.M., Moisander P.H., Niggemann J., Dittmar T., Duhamel S., Grosso O., Pujo-Pay M., Hélias-Nunige S., and S. Bonnet "Aphotic N2 fixation along an oligotrophic to ultraoligotrophic transect in the Western Tropical South Pacific Ocean" Biogeosciences , v.15 , 2018 , p.3107 10.5194/bg-15-3107-2018
Dupouy C., Frouin R., Tedetti M., Maillard M., Rodier M., Lombard F., Guidi L., Picheral M., Duhamel S., Charrière B., and R. Sempéré "Diazotrophic Trichodesmium influence on ocean color and pigment composition in the South West tropical Pacific" Biogeosciences , v.15 , 2018 , p.5249 10.5194/bg-15-5249-2018
Rousselet L., de Verneil A., Doglioli A.M., Petrenko A.A., Duhamel S., Maes C., and B. Blanke "Large- to submesoscale surface circulation and its implications on biogeochemical/biological horizontal distributions during the OUTPACE cruise (southwest Pacific)" Biogeosciences , v.15 , 2018 , p.2411 10.5194/bg-15-2411-2018
Bock, Nicholas and Van Wambeke, France and Dion, Moïra and Duhamel, Solange "Microbial community structure in the western tropical South Pacific" Biogeosciences , v.15 , 2018 10.5194/bg-15-3909-2018 Citation Details
Duhamel S., Van Wambeke F., Lefevre D., Benavides M., and S. Bonnet "Mixotrophic metabolism by natural communities of unicellular cyanobacteria in the western tropical South Pacific Ocean" Environmental Microbiology , v.20 , 2018 , p.2743 10.1111/1462-2920.14111
Van Wambeke, France and Gimenez, Audrey and Duhamel, Solange and Dupouy, Cécile and Lefevre, Dominique and Pujo-Pay, Mireille and Moutin, Thierry "Dynamics and controls of heterotrophic prokaryotic production in the western tropical South Pacific Ocean: links with diazotrophic and photosynthetic activity" Biogeosciences , v.15 , 2018 10.5194/bg-15-2669-2018 Citation Details
Rabouille, Sophie and Tournier, Lauralie and Duhamel, Solange and Claquin, Pascal and Crispi, Olivier and Talec, Amélie and Landolfi, Angela and Oschlies, Andreas "Organic Phosphorus Scavenging Supports Efficient Growth of Diazotrophic Cyanobacteria Under Phosphate Depletion" Frontiers in Microbiology , v.13 , 2022 https://doi.org/10.3389/fmicb.2022.848647 Citation Details
Bock N.A., Van Wambeke F., Dion M., and S. Duhamel "Microbial community structure in the western tropical South Pacific" Biogeosciences , v.15 , 2018 , p.3909 10.5194/bg-15-3909-2018
Benavides, Mar and Shoemaker, Katyanne M. and Moisander, Pia H. and Niggemann, Jutta and Dittmar, Thorsten and Duhamel, Solange and Grosso, Olivier and Pujo-Pay, Mireille and Hélias-Nunige, Sandra and Fumenia, Alain and Bonnet, Sophie "Aphotic N<sub>2</sub> fixation along an oligotrophic to ultraoligotrophic transect in the western tropical South Pacific Ocean" Biogeosciences , v.15 , 2018 10.5194/bg-15-3107-2018 Citation Details
Rousselet, Louise and de Verneil, Alain and Doglioli, Andrea M. and Petrenko, Anne A. and Duhamel, Solange and Maes, Christophe and Blanke, Bruno "Large- to submesoscale surface circulation and its implications on biogeochemical/biological horizontal distributions during the OUTPACE cruise (southwest Pacific)" Biogeosciences , v.15 , 2018 10.5194/bg-15-2411-2018 Citation Details
(Showing: 1 - 10 of 20)

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.

This project aimed to improve our understanding of marine cyanobacteria utilization of organic matter. A major goal was to characterize the role of light in organic molecules (carbon and nutrients) assimilation and the importance of mixotrophy (also called photoheterotrophy) within cyanobacteria metabolism.

 

Marine cyanobacteria, the most abundant marine phytoplankton, have a major role in shaping nutrients cycling and are major contributors to primary production and carbon export in the open ocean. Marine cyanobacteria are considered to be photoautotrophic (use light for energy and CO2 as a source of carbon), but recent evidence suggests they may also benefit from assimilation of organic molecules, including single carbon containing molecules, and may therefore be mixotrophic (capable of using inorganic and organic carbon sources). However, their mixotrophic metabolism is still poorly understood. Before this project, most studies investigating the light-dependent organic carbon uptake potential of marine cyanobacteria had been performed with cultures, while only one field study had demonstrated glucose uptake by Prochlorococcus in the Atlantic Ocean. Hence, in situ data was lacking to assess the potential mixotrophic nutrition of these globally relevant marine cyanobacteria, how it compares to their autotrophic nutrition mode (CO2 fixation), and its environmental controls (nutrients, light levels, etc.).

 

Using a combination of innovative approaches, which leveraged cruises of opportunity we confirmed that natural marine cyanobacteria of the genus Prochlorococcus and Synechococcus can incorporate organic molecules with variable C:N:P composition, including glucose, a single C-containing molecule. In fact, mixotrophy by these unicellular cyanobacteria was widespread over a wide range of biogeochemically distinct regions of the Western Tropical South Pacific Ocean and the North Pacific subtropical gyre. We similarly found that organic molecules could also be directly taken up by the nitrogen-fixing filamentous cyanobacteria Trichodesmium or primarily consumed by heterotrophic bacteria colonizing its surface, that ultimately transfer reduced organic compounds to their host. Therefore, our results showed that mixotrophy is widespread among unicellular and filamentous groups of marine cyanobacteria, nitrogen fixers and non-nitrogen fixers, and across ocean basins. However, based on group specific measurements of carbon assimilation from CO2 or glucose, we demonstrated that Prochlorococcus and Synechococcus, remain primarily photoautotrophic. Our findings indicate that mixotrophy by marine cyanobacteria is more likely to be an adaptation to low inorganic nutrient availability rather than a facultative pathway for carbon acquisition.

 

Additional critical gaps in our understanding of cyanobacteria mixotrophic metabolism concern regulating factors. In particular, how organic C assimilation by marine unicellular cyanobacteria depends upon light availability and photosynthetic electron transport in natural settings. We showed that assimilation rates of organic molecules are reduced in the dark or when photosynthesis is impaired, meaning that this mixotrophic metabolism is likely dependent on light energy fueling photosynthesis. In follow-up experiments we demonstrated that the uptake of glucose by natural cyanobacteria responds to light intensity similarly to photosynthesis and follows a diel pattern.

 

Finally, we found that over a third of the total leucine uptake was by the Prochlorococcus group. This is important because bacterial production, a fundamental parameter for biological oceanography, is commonly measured based on the incorporation of leucine in bacterial proteins. Therefore, we recommend that the contribution of picocyanobacteria to bacterial production estimates should be considered when measuring bacterial production in marine environments, even in dark incubations.

 

Overall these results suggest that dissolved organic matter utilization provides nutritional plasticity to marine cyanobacteria in oligotrophic environments. Results from the project have been published in peer-reviewed journals (eight manuscripts as of November 2018, plus several in preparation), and disseminated through presentations at scientific meetings and databases. This research stimulated new international collaborations. A video was created for the large public to learn about an international research cruise that was key to this project (OUTPACE: Oligotrophy to UlTra-oligotrophy PACific Experiment). Our findings have also been shared with high school teachers for diffusion to their classroom, and to many public outreach events at sciences fairs, science festivals and open houses in museums and at Columbia University. This project supported an early career female scientist, a graduate student, two Bachelor theses from female students and several undergraduate and high school students.

 


Last Modified: 10/30/2018
Modified by: Solange Duhamel

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

Print this page

Back to Top of page