The balance between photosynthesis and respiration explains the niche differentiation between Crocosphaera and Cyanothece
Status PubMed-not-MEDLINE Jazyk angličtina Země Nizozemsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
36514336
PubMed Central
PMC9732122
DOI
10.1016/j.csbj.2022.11.029
PII: S2001-0370(22)00525-6
Knihovny.cz E-zdroje
- Klíčová slova
- Carbon consumption, Niche separation, UCYN-B, UCYN-C,
- Publikační typ
- časopisecké články MeSH
Crocosphaera and Cyanothece are both unicellular, nitrogen-fixing cyanobacteria that prefer different environments. Whereas Crocosphaera mainly lives in nutrient-deplete, open oceans, Cyanothece is more common in coastal, nutrient-rich regions. Despite their physiological similarities, the factors separating their niches remain elusive. Here we performed physiological experiments on clone cultures and expand upon a simple ecological model to show that their different niches can be sufficiently explained by the observed differences in their photosynthetic capacities and rates of carbon (C) consumption. Our experiments revealed that Cyanothece has overall higher photosynthesis and respiration rates than Crocosphaera. A simple growth model of these microorganisms suggests that C storage and consumption are previously under-appreciated factors when evaluating the occupation of niches by different marine nitrogen fixers.
Balaton Limnological Research Institute Eötvös Loránd Research Network Tihany Hungary
Cellular Imaging Laboratory Biological Research Center Eötvös Loránd Research Network Szeged Hungary
Graduate School of Oceanography University of Rhode Island Narragansett RI 02882 USA
Institute of Microbiology The Czech Academy of Sciences Opatovický mlýn 37901 Třeboň Czech Republic
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Bergman B., Gallon J.R., Rai A.N., Stal L.J. N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev. 1997;19:139–185.
Bonnet S., Berthelot H., Turk-Kubo K., Fawcett S., Rahav E., Helguen S., Berman-Frank I. 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. 2016;13:2653–2673.
Breitbarth E., Mills M.M., Friedrichs G., LaRoche J. The Bunsen gas solubility coefficient of ethylene as a function of temperature and salinity and its importance for nitrogen fixation assays. Limnol. Oceanogr.-Methods. 2004;2:282–288.
Caputo A, Nylander JAA, Foster RA. The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration. FEMS Microbiol Lett 2019;366. PubMed PMC
Carpenter E.J., Janson S. Intracellular symbionts in the marine diatom Climacodium frauenfeldianum Grunow (Bacillariophyceae) J Physiol. 2000;36:540–544. PubMed
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. 2013;110:13210–13215. PubMed PMC
Chen Y.B., Zehr J.P., Mellon M. Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101 in defind media: evidence for a circadian rhythm. J Phycol. 1996;32:916–923.
Dron A., Rabouille S., Claquin P., Chang P., Raimbault V., Talec A., et al. Light:dark (12:12 h) quantification of carbohydrate fluxes in Crocosphaera watsonii. Aquat Microb Ecol. 2012;68:43–55.
du Plooy S.J., Carrasco N.K., Perissinotto R. Effects of zooplankton grazing on the bloom-forming Cyanothece sp. in a subtropical estuarine lake. J Plankton Res. 2017;39:826–835.
Dugenne M., Henderikx Freitas F., Wilson S.T., Karl D.M., White A.E. Life and death of Crocosphaera sp. in the Pacific Ocean: Fine scale predator–prey dynamics. Limnol Oceanogr. 2020;9999:1–15. PubMed
Eilers P.H.C., Peeters J.C.H. A model for the relationship between light-intensity and the rate of photosynthesis in phytoplankton. Ecol Model. 1988;42:199–215.
Fay P. Oxygen relations of nitrogen-fixation in cyanobacteria. Microbiology Reviews. 1992;56:340–373. PubMed PMC
Flores E, Herrero A. In The Molecular Biology of Cyanobacteria (Bryant, D.A., ed.), pp. 487–517, Kluwer Scientific Publications, Dordrecht, The Netherlands; 1994.
Gallon J.R. Reconciling the incompatible: N2 fixation and oxygen. New Phytol. 1992;122:571–609.
Gruber N. The marine nitrogen cycle: Overview and challenges. Nitrogen in the marine environment. 2008;2:1–50.
Gruber N., Galloway J.N. An Earth-system perspective of the global nitrogen cycle. Nature. 2008;451:293–296. PubMed
Holm-Hansen O, Helbling E. Técnicas para la medición de la productividad primaria en el fitoplancton in Manual de Métodos Ficológicos, ed. K. Alveal, M.E. Ferrario, E.C. Oliveira, E. Sar (Concepción, Universidad de Concepción); 1995. pp. 329–350.
Inomura K., Omta A.W., Talmy D., Bragg J., Deutsch C., Follows M.J. A Mechanistic Model of Macromolecular Allocation, Elemental Stoichiometry, and Growth Rate in Phytoplankton. Front Microbiol. 2020;11:86. PubMed PMC
Inomura K., Deutsch C., Wilson S.T., Masuda T., Lawrenz E., Lenka B., et al. Quantifying oxygen management and temperature and light dependencies of nitrogen fixation by Crocosphaera watsonii. mSphere. 2019;4 e00531-00519. PubMed PMC
Inomura K., Masuda T., Eichner M., Rabouille S., Zavřel T., Červený J., et al. Quantifying Cyanothece growth under DIC limitation. Comput Struct Biotechnol J. 2021;19:6456–6464. PubMed PMC
Komenda J., Knoppova J., Kopecna J., Sobotka R., Halada P., Yu J., et al. The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 2012;158:476–486. PubMed PMC
Lawrenz E., Silsbe G., Capuzzo E., Ylostalo P., Forster R.M., Simis S.G., et al. Predicting the electron requirement for carbon fixation in seas and oceans. PLoS One. 2013;8:e58137. PubMed PMC
Mareš J., Johansen J.R., Hauer T., Zima J., Jr., Ventura S., Cuzman O., et al. Taxonomic resolution of the genus Cyanothece (Chroococcales, Cyanobacteria), with a treatment on Gloeothece and three new genera, Crocosphaera, Rippkaea, and Zehria. J Phycol. 2019;55:578–610. PubMed
Masuda T., Inomura K., Mares J., Prasil O. Crocosphaera watsonii. Trends Microbiol. 2022 PubMed
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. 2013;58:2029–2036.
Masuda T., Bernat G., Beckova M., Kotabova E., Lawrenz E., Lukes M., et al. Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ Microbiol. 2018;20:546–560. PubMed
Moisander P.H., Beinart R.A., Hewson I., White A.E., Johnson K.S., Carlson C.A., et al. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science. 2010;327:1512–1514. PubMed
Montoya J.P., Voss M., Kahler P., Capone D.G. A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Appl Environ Microbiol. 1996;62:986–993. PubMed PMC
Nedbal L., Trtilek M., Cerveny J., Komarek O., Pakrasi H.B. A photobioreactor system for precision cultivation of photoautotrophic microorganisms and for high-content analysis of suspension dynamics. Biotechnol Bioeng. 2008;100:902–910. PubMed
Oxborough K., Moore C.M., Suggett D.J., Lawson T., Chan H.G., Geider R.J. Direct estimation of functional PSII reaction center concentration and PSII electron flux on a volume basis: a new approach to the analysis of Fast Repetition Rate fluorometry (FRRf) data. Limnol Oceanogr Method. 2012;10:142–154.
Polerecky L., Masuda T., Eichner M., Rabouille S., Vancová M., Kienhuis M.V.M., et al. Temporal patterns and intra- and inter-cellular variability in carbon and nitrogen assimilation by the unicellular cyanobacterium Cyanothece sp. ATCC 51142. Front Microbiol. 2021;12 PubMed PMC
Provasoli L., McLaughlin J.J., Droop M.R. The development of artificial media for marine algae. Arch Mikrobiol. 1957;25:392–428. PubMed
Rabouille S., Claquin P. Photosystem-II shutdown evolved with nitrogen fixation in the unicellular diazotroph Crocosphaera watsonii. Environ Microbiol. 2016;18:477–485. PubMed
Rabouille S., Campbell D.A., Masuda T., Zavrel T., Bernat G., Polerecky L., et al. Electron and biomass dynamics of Cyanothece under interacting nitrogen and carbon limitations. Front Microbiol. 2021;617802 PubMed PMC
Reddy KJ, Haskell JB, DM, S, LA, S. Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 1993;175:1284–1292. PubMed PMC
Schneegurt M.A., Sherman D.M., Nayar S., Sherman L.A. Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp. strain ATCC 51142. J Bacteriol. 1994;176:1586–1597. PubMed PMC
Shiozaki T., Kondo Y., Yuasa D., Takeda S. Distribution of major diazotrophs in the surface water of the Kuroshio from northeastern Taiwan to south of mainland Japan. J Plankton Res. 2018;40:407–419.
Sicora C.I., Chis I., Chis C., Sicora O. Regulation of PSII function in Cyanothece sp. ATCC 51142 during a light-dark cycle. Photosynth Res. 2019;139:461–473. PubMed
Sohm J.A., Webb E.A., Capone D.G. Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol. 2011;9:499–508. PubMed
Tang W., Cassar N. Data-driven modeling of the distribution of diazotrophs in the global ocean. Geophys Res Lett. 2019;46:12258–12269.
Turk-Kubo K.A., Frank I.E., Hogan M.E., Desnues A., Bonnet S., Zehr J.P. Diazotroph community succession during the VAHINE mesocosm experiment (New Caledonia lagoon) Biogeosciences. 2015;12:7435–7452.
Webb E.A., Ehrenreich I.M., Brown S.L., Valois F.W., Waterbury J.B. Phenotypic and genotypic characterization of multiple strains of the diazotrophic cyanobacterium, Crocosphaera watsonii, isolated from the open ocean. Environ Microbiol. 2009;11:338–348. PubMed
Wilson S.T., Aylward F.O., Ribalet F., Barone B., Casey J.R., Connell P.E., et al. Coordinated regulation of growth, activity and transcription in natural populations of the unicellular nitrogen-fixing cyanobacterium Crocosphaera. Nat Microbiol. 2017;2:17118. PubMed
Zehr J.P., Capone D.G. Changing perspectives in marine nitrogen fixation. Science. 2020;368 PubMed
Zehr J.P., Waterbury J.B., Turner P.J., Montoya J.P., Omoregie E., Steward G.F., et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacifc Ocean. Nature. 2001;412:635–638. PubMed
Capone D.G., Montoya J.P. Nitrogen fixation and denitrification. Methods Microbiol. 2001;30:501–515.
The biogenesis and maintenance of PSII: Recent advances and current challenges