Montoya, J. P., Carpenter, E. J. & Capone, D. G. Nitrogen fixation and nitrogen isotope abundances in zooplankton of the oligotrophic North Atlantic. Limnol. Oceanogr. 47, 1617–1628 (2002).
Hunt, B. P. V. et al. Contribution and pathways of diazotroph-derived nitrogen to zooplankton during the VAHINE mesocosm experiment in the oligotrophic New Caledonia lagoon. Biogeosciences 13, 3131–3145 (2016).
Horii, S., Takahashi, K., Shiozaki, T., Hashihama, F. & Furuya, K. Stable isotopic evidence for the differential contribution of diazotrophs to the epipelagic grazing food chain in the mid-Pacific Ocean. Glob. Ecol. Biogeogr. 27, 1467–1480 (2018).
Loick-Wilde, N. et al. Nitrogen sources and net growth efficiency of zooplankton in three Amazon River plume food webs. Limnol. Oceanogr. 61, 460–481 (2016).
Kuypers, M. M. M., Marchant, H. K. & Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 16, 263–276 (2018).
Gallon, J. R. Reconciling the incompatible: N2 fixation and oxygen. N. Phytol. 122, 571–609 (1992).
Fay, P. Oxygen relations of nitrogen-fixation in Cyanobacteria. Microbiol Rev. 56, 340–373 (1992).
Berman-Frank, I. et al. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine Cyanobacterium Trichodesmium. Science 294, 1534–1537 (2001).
Berman-Frank, I., Lundgren, P. & Falkowski, P. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res. Microbiol. 154, 157–164 (2003).
Sohm, J. A., Webb, E. A. & Capone, D. G. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol 9, 499–508 (2011).
Moisander, P. H. et al. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327, 1512–1514 (2010).
Luo, Y. W. et al. Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates. Earth Syst. Sci. Data 4, 47–73 (2012).
Monteiro, F. M., Follows, M. J. & Dutkiewicz, S. Distribution of diverse nitrogen fixers in the global ocean. Glob. Biogeochemical Cycles 24, GB3017 (2010).
Zehr, J. P. Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19, 162–173 (2011).
Zehr, J. P. & Bombar, D. Marine nitrogen fixation: organisms, significance, enigmas, and future directions. In Biological nitrogen fixation (ed. FJ de Bruijn) 857–872 (Wiley, 2015).
Zehr, J. P. et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635–638 (2001).
Foster, R. A., Sztejrenszus, S. & Kuypers, M. M. Measuring carbon and N2 fixation in field populations of colonial and free-living unicellular cyanobacteria using nanometer-scale secondary ion mass spectrometry. J. Phycol. 49, 502–516 (2013).
Montoya, J. P. et al. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027–1032 (2004).
Langlois, R. J., Hummer, D. & LaRoche, J. Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl Environ. Microbiol 74, 1922–1931 (2008).
Mohr, W., Intermaggio, M. P. & LaRoche, J. Diel rhythm of nitrogen and carbon metabolism in the unicellular, diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ. Microbiol 12, 412–421 (2010).
Dron, A. et al. Light:dark (12:12 h) quantification of carbohydrate fluxes in Crocosphaera watsonii. Aquat. Microb. Ecol. 68, 43–55 (2012).
Masuda, T. et al. Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ. Microbiol. 20, 546–560 (2018).
Mohr, W., Vagner, T., Kuypers, M. M., Ackermann, M. & La Roche, J. Resolution of conflicting signals at the single-cell level in the regulation of cyanobacterial photosynthesis and nitrogen fixation. PLoS ONE 8, e66060 (2013).
Langlois, R. J., LaRoche, J. & Raab, P. A. Diazotrophic diversity and distribution in the tropical and subtropical Atlantic Ocean. Appl. Environ. Microbiol. 71, 7910–7919 (2005).
Foster, R. A. et al. Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical north Atlantic Ocean. Limnol. Oceanogr. 52, 517–532 (2007).
Bonnet, S. et al. Dynamics of N2 fixation and fate of diazotroph-derived nitrogen in a low-nutrient, low-chlorophyll ecosystem: results from the VAHINE mesocosm experiment (New Caledonia). Biogeosciences 13, 2653–2673 (2016).
Reddy, K. J., Haskell, B., Sherman, D. M. & Sherman, L. A. Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J. Bacteriol. 175, 1284–1292 (1993).
Červený, J., Sinetova, M. A., Valledor, L., Sherman, L. A. & Nedbal, L. Ultradian metabolic rhythm in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Proc. Natl. Acad. Sci. USA 110, 13210–13215 (2013).
Tuit, C., Waterbury, J. & Ravizzaz, G. Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria. Limnol. Oceanogr. 49, 978–990 (2004).
Colón-López, M., Sherman, D. M. & Sherman, L. A. Transcriptional and translational regulation of nitrogenase in light-dark- and continuous-light grown cultures of the unicellular cyanobacterium Cyanothece sp. strain ATCC 51142. J. Bacteriol. 179, 4319–4327 (1997).
Pennebaker, K., Mackey, K. R. M., Smith, R. M., Williams, S. B. & Zehr, J. P. Diel cycling of DNA staining and nifH gene regulation in the unicellular cyanobacterium Crocosphaera watsonii strain WH 8501 (Cyanophyta). Environ. Microbiol. 12, 1001–1010 (2010).
Wagner, M. Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu. Rev. Microbiol. 63, 411–429 (2009).
Musat, N., Foster, R., Vagner, T., Adam, B. & Kuypers, M. M. Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol. Rev. 36, 486–511 (2012).
Popa, R. et al. Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME J. 1, 354–360 (2007).
Finzi-Hart, J. A. et al. Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry. Proc. Natl. Acad. Sci. USA 106, 9931–9931 (2009).
Marchant, H. K., Mohr, W. & Kuypers, M. M. Recent advances in marine N-cycle studies using 15N labeling methods. Curr. Opin. Biotechnol. 41, 53–59 (2016).
Martínez-Pérez, C. et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat. Microbiol. 1, 16163 (2016).
Krupke, A. et al. The effect of nutrients on carbon and nitrogen fixation by the UCYN-A–haptophyte symbiosis. ISME J. 9, 1635–1647 (2015).
Iversen, G. R. Analysis of variance. In: International Encyclopedia of Statistical Science (ed. Lovric M.) (Springer, Berlin, Heidelberg, 2011).
Bandyopadhyay, A., Elvitigala, T., Liberton, M. & Pakrasi, H. B. Variations in the rhythms of respiration and nitrogen fixation in members of the unicellular diazotrophic cyanobacterial genus Cyanothece. Plant Physiol. 161, 1334–1346 (2013).
Stȩpniak, C. Coefficient of variation. In: International Encyclopedia of Statistical Science (ed. Lovric M.) (Springer, Berlin, Heidelberg, 2011).
Zhang, C., Mapes, B. E. & Soden, B. J. Bimodality in tropical water vapour. Q. J. R. Meteorological Soc. 129, 2847–2866 (2003).
Großkopf, T. & Laroche, J. Direct and indirect costs of dinitrogen fixation in Crocosphaera watsonii WH8501 and possible implications for the nitrogen cycle. Front. Microbiol. 3, 236 (2012).
Inomura, K., Bragg, J. & Follows, M. J. A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii. ISME J. 11, 166–175 (2017).
Rittmann, B. E. & McCarty, P. L. Stoichiometry and bacterial energetics. In: Environmental Biotechnology: Principles and Applications. 126–164 (McGraw-Hill, New York, NY, USA, 2001).
Fu, F. X. et al. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol. Oceanogr. 53, 2472–2484 (2008).
Gradoville, M. R., White, A. E. & Letelier, R. M. Physiological response of Crocosphaera watsonii to enhanced and fluctuating carbon dioxide conditions. PLoS ONE 9, e110660 (2014).
Follett, C. L., Dutkiewicz, S., Karl, D. M., Inomura, K. & Follows, M. J. Seasonal resource conditions favor a summertime increase in North Pacific diatom-diazotroph associations. ISME J. 12, 1543–1557 (2018).
Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) Program: Background, rationale and field implementation. Deep-Sea Res. 43, 129–156 (1996).
Shiozaki, T. et al. Linkage between dinitrogen fixation and primary production in the oligotrophic South Pacific Ocean. Glob. Biogeochem. Cycles 32, 1028–1044 (2018).
Dekaezemacker, J. & Bonnet, S. Sensitivity of N2 fixation to combined nitrogen forms (NO3− and NH4+) in two strains of the marine diazotroph Crocosphaera watsonii (Cyanobacteria). Mar. Ecol. Prog. Ser. 438, 33–46 (2011).
Knapp, A. N., Dekaezemacker, J., Bonnet, S., Sohm, J. A. & Capone, D. G. Sensitivity of Trichodesmium erythraeum and Crocosphaera watsonii abundance and N2 fixation rates to varying NO3− and PO43− concentrations in batch cultures. Aquat. Microb. Ecol. 66, 223–236 (2012).
Knapp, A. N. The sensitivity of marine N2 fixation to dissolved inorganic nitrogen. Front Microbiol 3, 374 (2012).
Inomura, K., Bragg, J., Riemann, L. & Follows, M. J. A quantitative model of nitrogen fixation in the presence of ammonium. PLoS ONE 13, e0208282 (2018).
Stukel, M. R., Coles, V. J., Brooks, M. T. & Hood, R. R. Top-down, bottom-up and physical controls on diatom-diazotroph assemblage growth in the Amazon River plume. Biogeosciences 11, 3259–3278 (2014).
Dutkiewicz, S. et al. Capturing optically important constituents and properties in a marine biogeochemical and ecosystem model. Biogeosciences 12, 4447–4481 (2015).
Ackermann, M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat. Rev. Microbiol 13, 497–508 (2015).
Celiker, H. & Gore, J. Cellular cooperation: insights from microbes. Trends Cell Biol. 23, 9–15 (2013).
Lin, S., Henze, S., Lundgren, P., Bergman, B. & Carpenter, E. J. Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 64, 3052–3058 (1998).
Kupper, H., Ferimazova, N., Setlik, I. & Berman-Frank, I. Traffic lights in trichodesmium. Regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Plant Physiol. 135, 2120–2133 (2004).
Eichner, M. J. et al. Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO2. ISME J. 11, 1305–1317 (2017).
Ohki, K. & Taniuchi, Y. Detection of nitrogenase in individual cells of a natural population of Trichodesmium using immunocytochemical methods for fluorescent cells. J. Oceanogr. 65, 427–432 (2009).
Sanchez-Baracaldo, P., Hayes, P. K. & Blank, C. E. Morphological and habitat evolution in the Cyanobacteria using a compartmentalization approach. Geobiology 3, 145–165 (2005).
Hammerschmidt, K., Landan, G., Kümmel Tria, F. D. & Dagan, T. A chronology of multicellularity evolution in cyanobacteria. bioRxiv https://doi.org/10.1101/570788 (2019).
Schirrmeister, B. E., Antonelli, A. & Bagheri, H. C. The origin of multicellularity in cyanobacteria. BMC Evolut. Biol. 11, 45 (2011).
Kirk, D. L. A twelve-step program for evolving multicellularity and a division of labor. BioEssays 27, 299–310 (2005).
Michod, R. E. Evolution of individuality during the transition from unicellular to multicellular life. Proc. Natl. Acad. Sci. USA 104, 8613–8618 (2007).
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. Limnol. Oceanogr. 58, 2029–2036 (2013).
Guillard, R. R. L. & Ryther, J. H. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can. J. Microbiol. 8, 229–239 (1962).
Guillard, R. R. L. Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals (eds Smith W.L. & Chanley M.H) 26–60 (Plenum Press, New York, USA, 1975).
Provasoli, L., McLaughlin, J. J. A. & Droop, M. R. The development of artificial media for marine algae. Arcb. Mikrobiol. 25, 392–428 (1957).
Shiozaki, T. et al. Why is Trichodesmium abundant in the Kuroshio? Biogeosciences 12, 6931–6943 (2015).
Musat, N. et al. A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc. Natl. Acad. Sci. USA 105, 17861–17866 (2008).
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
Chavez, F. P., Messie, M. & Pennington, J. T. Marine primary production in relation to climate variability and change. Ann. Rev. Mar. Sci. 3, 227–260 (2011).
Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H. & Teller, E. Equation of state calculations by fast computing machines. J. Chem. Phys. 21, 1087–1092 (1953).
Omta, A. W. et al. Extracting phytoplankton physiological traits from batch and chemostat culture data. Limnol. Oceanogr.: Methods 15, 453–466 (2017).
Krishnamoorthy, K. Statistical distributions: an overview. In International Encyclopedia of Statistical Science (ed. Lovric M.) (Springer, Berlin, Heidelberg, 2011).
Wilson, E. B. & Hilferty, M. M. The distribution of chi-square. Proc. Natl. Acad. Sci. USA 17, 684–688 (1931).
Sohm, J. A., Edwards, B. R., Wilson, B. G. & Webb, E. A. Constitutive extracellular polysaccharide (EPS) production by specific isolates of Crocosphaera watsonii. Front Microbiol 2, 229 (2011).
Benson, B. B. & Krause, D. The concentration and isotopic fraction of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnol. Oceanogr. 29, 620–632 (1984).
Ågren, G. I. The C:°N:°P stoichiometry of autotrophs – theory and observations. Ecol. Lett. 7, 185–191 (2004).
Pahlow, M. & Oschlies, A. Chain model of phytoplankton P, N and light colimitation. Mar. Ecol. Prog. Ser. 376, 69–83 (2009).
Talmy, D., Blackford, J., Hardman-Mountford, N. J., Dumbrell, A. J. & Geider, R. J. An optimality model of photoadaptation in contrasting aquatic light regimes. Limnol. Oceanogr. 58, 1802–1818 (2013).
Geider, R. J., MacIntyre, H. L. & Kana, T. M. A dynamic regulatory model of phytoplanktonic acclimation to light, nutrients, and temperature. Limnol. Oceanogr. 43, 679–694 (1998).
Ghyoot, C., Flynn, K. J., Mitra, A., Lancelot, C. & Gypens, N. Modeling plankton mixotrophy: a mechanistic model consistent with the Shuter-type biochemical approach. Front. Ecol. Evol. 5, https://doi.org/10.3389/fevo.2017.00078 (2017).
Cullen, J. J. On models of growth and photosynthesis in phytoplankton.Deep Sea Res. 37, 667–683 (1989).
Letelier, R. M., Karl, D. M., Abbott, M. R. & Bidigare, R. R. Light driven seasonal patterns of chlorophyll and nitrate in the lower euphotic zone of the North Pacific Subtropical Gyre. Limnol. Oceanogr. 49, 508–519 (2004).
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