Predicting how O2 characterizes the niche of marine unicellular diazotroph Crocosphaera

Keisuke Inomura1, Curtis A. Deutsch2, Samuel T Wilson3, Takako Masuda4, Evelyn Lawrenz4, Bučinská Lenka5, Roman Sobotka5, Julia Gauglitz6, Mak A Saito7, Ondřej Prášil4, Naoto Takahata8, Takuhei Shiozaki9, Yuji Sano10, Ken Furuya and Michael J Follows12, (1)University of Washington Seattle, Seattle, United States, (2)University of Washington Seattle Campus, School of Oceanography, Seattle, United States, (3)Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii at Manoa, Honolulu, HI, United States, (4)Institute of Microbiology, Czech Academy of Sciences, Center Algatech, Třeboň, Czech Republic, (5)Institute of Microbiology, Czech Academy of Sciences, Czech Republic, (6)Woods Hole Oceanographic Institution, Marine Chemistry and Geochemistry, Woods Hole, MA, United States, (7)Woods Hole Oceanographic Institution, Marine Chemistry and Geochemistry, Woods Hole, United States, (8)University of Tokyo, Atmosphere and Ocean Research Institute, Kashiwa, Japan, (9)The University of Tokyo, Tokyo, Japan, (10)Marie Core Research Institute, Kochi University, Nankoku, Japan, (11)Massachusetts Institute of Technology, Department of Earth, Atmospheric and Planetary Sciences, Cambridge, United States
Crocosphaera is a major marine unicellular nitrogen fixer, providing bioavailable nitrogen essential to marine ecosystem productivity. A major energetic cost of N2 fixation stems from the need to maintain low intracellular O2, in surface ocean habitats where O2 is abundant, yet these costs are poorly understood. We present a mechanistic model of cellular metabolisms (Cell Flux Model) resolving C, N and O2 fluxes to show how the energetic costs of O2 management constrain their ecological niche and biogeographic distribution. The model shows that Crocosphaera combines multiple strategies to manage intracellular O2: respiratory protection, size adjustment, and low diffusivity membranes. Even with this combination of strategies, the level of respiratory protection is only sufficient at high temperature, explaining why the geographic range of Crocosphaera is limited to waters warmer than 20 ºC. Since the respiratory protection is costly in C, management of O2 requires high rates of photosynthesis, constraining the depths with sufficient light for Crocosphaera. However, we show that such C cost can be reduced by the formation of cell colonies with a division of metabolic roles in which only a fraction of cells fix nitrogen with respiratory protection. These quantified niche constraints provide useful implication in predicting hot spots of nitrogen fixation in the oligotrophic ocean.