Nitrogen fixing plankton provide nitrogen to fuel marine ecosystems and biogeochemical cycles but the factors that constrain their growth and habitat remain poorly understood. Here we investigate the importance of metabolic specialization in unicellular diazotroph populations, using laboratory experiments and model simulations. In clonal cultures of Crocosphaera watsonii and Cyanothece sp. spiked with 15N2, cellular 15N enrichment developed a bimodal distribution within colonies, indicating that N2 fixation was confined to a subpopulation. In a model of population metabolism, heterogeneous nitrogen (N2) fixation rates substantially reduce the respiration rate required to protect nitrogenase from O2. The energy savings from metabolic specialization is highest at slow growth rates, allowing populations to survive in deeper waters where light is low but nutrients are high. Our results suggest that heterogeneous N2 fixation in colonies of unicellular diazotrophs confers an energetic advantage that expands the ecological niche and may have facilitated the evolution of multicellular diazotrophs.

Atmosphere and Ocean Research Institute The University of Tokyo Kashiwanoha Kashiwa shi Chiba 277 8564 Japan

Department of Aquatic Bioscience The University of Tokyo Yayoi Bunkyo Tokyo 113 8657 Japan

Global Change Research Institute The Czech Academy of Sciences 664 24 Drásov Olomouc Czech Republic

Graduate School of Science and Engineering Soka University Tangi Hachioji Tokyo 192 8577 Japan

Institute of Microbiology The Czech Academy of Sciences Opatovický mlýn 379 01 Třeboň Czech Republic

School of Oceanography University of Washington Seattle WA USA

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Commun Biol. 2023 Jun 7;6(1):614. doi: 10.1038/s42003-023-05007-6. PubMed

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Temporal Patterns and Intra- and Inter-Cellular Variability in Carbon and Nitrogen Assimilation by the Unicellular Cyanobacterium Cyanothece sp. ATCC 51142

Quantitative models of nitrogen-fixing organisms