Some species of extant unicellular diazotrophic cyanobacteria (UCYN) such as Crocosphaera watsonii and Cyanothece spp. confine N2 fixation to night-time, when photosynthesis is “turned off”. We try to understand the mechanism underlying nocturnal inactivation of photosynthesis. Our data show that the decline in photosystem II activity and abundance was related to light-induced modification of photosystem II and suppressed synthesis of membrane proteins. We also tried to quantify the role of three O2 management strategies (size adjustment, reduced O2 diffusivity, and respiratory protection) by Crocosphaera watsonii. Our study shows that Crocosphaera increase their cell size and form a barrier for O2 along the cell wall by starch granules and thylakoid membranes under high O2. In addition, model results indicate a critical role for respiration in maintaining the N2 fixation rate.

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Inomura K., Deutsch C., Wilson S.T., Masuda T., Lawrenz E., Bučinská L., Sobotka R., Gauglitz J.M., Saito M.A., Prášil O., Follows. Quantifying oxygen management and temperature and light dependencies of nitrogen fixation by Crocosphaera watsonii. mSphere 4, e00531-19 (2019).

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Masuda T., Bernát G., Bečková M., Kotabová E., Lawrenz E., Lukeš M., Komenda J., Prášil O. Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ. Microbiol. 20, 546-560 (2018).

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N2 fixation is energetically expensive since it requires additional energy costs for the nocturnal respiration in order to make cells anaerobic. On the other hand, under conditions of sufficient light (i.e. near the surface of the ocean) and under ample supply of inorganic C, the cells can accumulate as much C reserves as their cell size allows. We try to understand the effect of the nitrogen source on energy budget and growth of N2 fixers.

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Conventionally, N2 fixation is considered to be inhibited in the presence of dissolved inorganic nitrogen, such as ammonium and nitrate. However, we have observed continuation of significant N2 fixation rates under conditions when ammonium was available in Crocosphaera. Later, a collaborative study with modelers revealed that Crocosphaera can increase their population and expand their niche despite the presence of ammonium. Further, our field observation data suggest Crocosphaera could be a major ammonium consumer in situ.

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Masuda T.*, Inomura K., Kodama T., Shiozaki T., Kitajima S., Armin G., Matsui T., Suzuki K, Takeda S., Prášil O., Furuya K. Crocosphaera as a major consumer of fixed nitrogen despite its capability of nitrogen fixation.  Microbiology Spectrum 10 (4), e02177-21 (2022)

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Inomura K., Masuda T., Gauglitz J.M. Active nitrogen fixation by Crocosphaera expands their niche despite the presence of ammonium – A case study. Scientific Reports 9, 15064 (2019)

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Masuda T., Furuya K., Kodama T., Takeda S., Harrison, P. J. Ammonium uptake and dinitrogen fixation by the unicellular nanocyanobacterium Crocosphaera watsoniiin nitrogen-limited continuous cultures. Limnology and Oceanography 58, 2029-2036 (2013)

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Microbial communities, including cyanobacteria, consist of a genetically diverse assembly of different organisms, and the level of genetic diversity plays an important part in community properties and functions. However, biological diversity also arises at a lower level of biological organization, between genetically identical cells that reside in the same microenvironment. Even when genetic and environmental differences between cells are reduced as much as possible, single cells differ from each other with respect to gene expression and other phenotypic traits. This phenotypic heterogeneity can have important functional consequences, similar to the consequences of the biological diversity that emerge at higher levels of biological organization. We have observed such heterogeneity in both Crocosphaera and Cyanothece. Our data show that N2 fixation is confined to subpopulation of cells. Model results show that this heterogeneity helps to reduce energy costs at population level, and indicate that heterogeneous N2 fixation may be a strategy to sustain a population in nutrient-limited environments.

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Polerecky L., Masuda T., Eichner M., Rabouille S., Vancová M., Kienhuis M.V.M., Bernát G., Bonomi-Barufi J., Campbell D.A., Claquin P., Červený J., Giordano M., Kotabová E., Kromkamp J., Lombardi A.T., Lukeš M., Prášil O., Stephan S., Suggett D., Zavřel T. and Halsey K.H.* Temporal patterns and intra- and inter-cellular variability in carbon and nitrogen assimilation by the unicellular cyanobacterium Cyanothece sp. ATCC51142. Frontiers in Microbiology. 12: 620915, https://doi.org/10.3389/fmicb.2021.620915

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Masuda T., Inomura K., Takahata N., Shiozaki T., Sano Y., Deutsch C., Prášil O., Furuya K., Heterogeneous N2 fixation rates confer energetic advantage and expanded ecological niche of unicellular diazotroph populations. Communications Biology, 3:172. https://doi.org/10.1038/s42003-020-0894-4 | www.nature.com/commsbio (2020)

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Prochlorococcus and Synechococcus are the two dominant picocyanobacteria in the nanomolar-level low-nutrient surface waters of the subtropical ocean, which support nearly a quarter of marine primary production. The geographical distributions of the two organisms are largely overlapping, but the basis for their coexistence in these biomes remains unclear. We combined in situ microcosm experiments, an ecosystem model and a phylogenomic analysis, and show that the coexistence of these two organisms can arise from specialization in the uptake of distinct nitrogen substrates. 

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Masuda T.*, Inomura K., Mareš J., Kodama T., Shiozaki T., Matsui T., Suzuki K., Takeda S., Deutsch C., Prášil O., Furuya K. Coexistence of dominant marine phytoplankton species sustained by nutrient specialization. Microbiology spectrum 11 (4), e04000-22 (2023)

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The oceans are warming and nutrient and light environments are changing. Since primary producers play a key role in the capacity of the world’s oceans to absorb anthropogenic carbon emissions (about 30% of anthropogenically derived CO2 have been entered the world’s oceans during the past two centuries), it is essential to predict how global change affects phytoplankton assemblages . Great efforts have been made to evaluate the effect of global change on growth and performance of photosynthetic organisms, due to their key importance as primary producers in the aquatic food webs, however, there are geographical regions that have been poorly explored. The Patagonian waters constitute one of the most important fishery areas of the Atlantic Ocean Basin, however, our knowledge about ecosystems, supporting aquatic food web in this area remains limited. To fill the knowledge gap, we try to evaluate the effect of global change on plankton assemblages in Patagonia, Argentina, in collaboration with Prof. Helbling W., Dr. Villafañe V. E. and Dr. Valiñas M.S at Estación de Fotobiología Playa Unión.

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Related publications---------------

Masuda T.*, Prášil O., Villafañe V.E., Valiñas M.S., Inomura K., Helbling E.W. Impact of increased nutrients and lowered pH on photosynthesis and growth of three marine phytoplankton communities from the coastal South West Atlantic (Patagonia, Argentina). Frontiers in Marine Science 8: 609962, https://doi.org/10.3389/fmars.2021.609962

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