Photoheterotrophy in unicellular cyanobacteria: ecological drivers and signigicance for marine biogeochemistry

DESCRIPTION: 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.

OUTCOMES: 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. doi: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. doi:10.5194/bg-15-3107-2018

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. doi:10.5194/bg-15-3909-2018

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. doi:10.1111/1462-2920.14111

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. doi:10.5194/bg-15-5249-2018

Van Wambeke F., Gimenez A., Duhamel S., Dupouy C., Lefevre D., Pujo-Pay M., and T. Moutin. "Dynamics and controls of heterotrophic prokaryotic production in the western tropical South Pacific Ocean: links with diazotrophic and photosynthetic activity," Biogeosciences, v.15, 2018, p. 2669. doi:10.5194/bg-15-2669-2018

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. doi:10.5194/bg-15-3909-2018 Citation details

Duhamel, Solange and Van Wambeke, France and Lefevre, Dominique and Benavides, Mar and Bonnet, Sophie. "Mixotrophic metabolism by natural communities of unicellular cyanobacteria in the western tropical South Pacific Ocean: Mixotrophy in natural marine cyanobacteria," Environmental Microbiology, v.20, 2018. doi:10.1111/1462-2920.14111 Citation details

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 N₂ fixation along an oligotrophic to ultraoligotrophic transect in the western tropical South Pacific Ocean," Biogeosciences, v.15, 2018. doi:10.5194/bg-15-3107-2018 Citation details

Dupouy, Cécile and Frouin, Robert and Tedetti, Marc and Maillard, Morgane and Rodier, Martine and Lombard, Fabien and Guidi, Lionel and Picheral, Marc and Neveux, Jacques and Duhamel, Solange and Charrière, Bruno and Sempéré, Richard. "Diazotrophic Trichodesmium impact on UV?Vis radiance and pigment composition in the western tropical South Pacific," Biogeosciences, v.15, 2018. doi:10.5194/bg-15-5249-2018 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. doi:10.5194/bg-15-2411-2018 Citation details

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. doi:10.5194/bg-15-2669-2018 Citation details

Benavides, Mar and Berthelot, Hugo and Duhamel, Solange and Raimbault, Patrick and Bonnet, Sophie. "Dissolved organic matter uptake by Trichodesmium in the Southwest Pacific," Scientific Reports, v.7, 2017. doi:10.1038/srep41315 Citation details

Berthelot H., Duhamel S., L?Helguen S., Maguer J.F., Wang S., and N. Cassar.. "NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton," The ISME Journal, 2018. doi:doi.org/10.1038/s41396-018-0285-8

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. doi:10.5194/bg-15-2411-2018