Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation

. 2008 ; 179 (3) : 784-798. [epub] 20080530

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid18513224

* As iron (Fe) deficiency is a main limiting factor of ocean productivity, its effects were investigated on interactions between photosynthesis and nitrogen fixation in the marine nonheterocystous diazotrophic cyanobacterium Trichodesmium IMS101. * Biophysical methods such as fluorescence kinetic microscopy, fast repetition rate (FRR) fluorimetry, and in vivo and in vitro spectroscopy of pigment composition were used, and nitrogenase activity and the abundance of key proteins were measured. * Fe limitation caused a fast down-regulation of nitrogenase activity and protein levels. By contrast, the abundance of Fe-requiring photosystem I (PSI) components remained constant. Total levels of phycobiliproteins remained unchanged according to single-cell in vivo spectra. However, the regular 16-kDa phycoerythrin band decreased and finally disappeared 16-20 d after initiation of Fe limitation, concomitant with the accumulation of a 20-kDa protein cross-reacting with the phycoerythrin antibody. Concurrently, nitrogenase expression and activity increased. Fe limitation dampened the daily cycle of photosystem II (PSII) activity characteristic of diazotrophic Trichodesmium cells. Further, it increased the number and prolonged the time period of occurrence of cells with elevated basic fluorescence (F(0)). Additionally, it increased the effective cross-section of PSII, probably as a result of enhanced coupling of phycobilisomes to PSII, and led to up-regulation of the Fe stress protein IsiA. * Trichodesmium survives short-term Fe limitation by selectively down-regulating nitrogen fixation while maintaining but re-arranging the photosynthetic apparatus.

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Behrenfeld MJ, Kolber ZS. 1999. Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283: 840-843.

Bergman B, Gallon JR, Rai AN, Stal LJ. 1997. N2 fixation by nonheterocystous cyanobacteria. FEMS Microbiology Reviews 19: 139-185.

Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG. 2004. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnology and Oceanography 49: 997-1005.

Berman-Frank I, Cullen JT, Shaked Y, Sherrell RM, Falkowski PG. 2001b. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnology and Oceanography 46: 1249-1260.

Berman-Frank I, Lundgren P, Chen Y-B, Küpper H, Kolber Z, Bergman B, Falkowski P. 2001a. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294: 1534-1537.

Berman-Frank I, Lundgren P, Falkowski P. 2003. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Research in Microbiology 154: 157-164.

Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G. 1998. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiology and Molecular Biology Reviews 62: 667-683.

Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T, Michaels AF, Carpenter EJ. 2005. Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochemical Cycles 19: doi 10.1029/2004GB002331.

Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221-1229.

Carpenter EJ, Roenneberg T. 1995. The marine planktonic cyanobacterium Trichodesmium spp.: photosynthetic rate measurements in the SW Atlantic Ocean. Marine Ecology Progress Series 118: 267-273.

Chen YB, Dominic B, Zani S, Mellon MT, Zehr JP. 1999. Expression of photosynthesis genes in relation to nitrogen fixation in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101. Plant Molecular Biology 41: 89-104.

Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP. 2005. Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Applied and Environmental Microbiology 71: 5362-5370.

Falkowski PG. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387: 272-275.

Fu FX, Bell PRF. 2003. Growth, N2 fixation and photosynthesis in a cyanobacterium, Trichodesmium sp., under Fe stress. Biotechnology Letter 25: 645-649.

Gallon JR. 1992. Reconciling the incompatible: N2 fixation and oxygen. New Phytologist 122: 571-609.

Gallon JR. 2001. N2 fixation in phototrophs: adaptation to a specialized way of life. Plant and Soil 230: 39-48.

Gao Y, Kaufman YJ, Tanre D, Kolber D, Falkowski PG. 2001. Seasonal distributions of aeolian iron fluxes to the global ocean. Geophysical Research Letters 28: 29-32.

Ihalainen JA, D’Haene S, Yeremenko N, Van Roon H, Arteni AA, Boekema EJ, Van Grondelle R, Matthijs HCP, Dekker JP. 2005. Aggregates of the chlorophyll-binding protein IsiA (CP43’) dissipate energy in cyanobacteria. Biochemistry 44: 10846-10853.

Janson S, Carpenter EJ, Bergman B. 1994. Compartmentalization of nitrogenase in a nonheterocystous cyanobacterium -Trichodesmium contortum. FEMS Microbiology Letters 118: 9-14.

Kana TM. 1993. Rapid oxygen cycling in Trichodesmium thiebautii. Limnology and Oceanography 38: 18-24.

Kolber ZS, Prasil O, Falkowski PG. 1998. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochimica et Biophysica Acta-Bioenergetics 1367: 88-106.

Kruskopf M, Du Plessis S. 2006. Growth and filament length of the bloom forming Oscillatoria simplicissima (Oscillatoriales, Cyanophyta) in varying N and P concentrations. Hydrobiologia 556: 357-362.

Küpper H, Aravind P, Leitenmaier B, Trtilek M, Šetlík I. 2007a. Cadmium-induced inhibition of photosynthesis and long-term acclimation to Cd-stress in the Cd hyperaccumulator Thlaspi caerulescens. New Phytologist 175: 655-674.

Küpper H, Ferimazova N, Šetlík I, Berman-Frank I. 2004. Traffic lights in Trichodesmium: regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Plant Physiology 135: 2120-2133.

Küpper H, Seibert S, Aravind P. 2007b. A fast, sensitive and inexpensive alternative to analytical pigment HPLC: quantification of chlorophylls and carotenoids in crude extracts by fitting with Gauss-Peak-Spectra. Analytical Chemistry 79: 7611-7627.

Küpper H, Šetlík I, Trtílek M, Nedbal L. 2000. A microscope for two-dimensional measurements of in vivo chlorophyll fluorescence kinetics using pulsed measuring light, continuous actinic light and saturating flashes. Photosynthetica 38: 553-570.

Kustka A, Sanudo-Wilhelmy S, Carpenter EJ, Capone DG, Raven JA. 2003. A revised estimate of the iron use efficiency of nitrogen fixation, with special reference to the marine cyanobacterium Trichodesmium spp. (Cyanophyta). Journal of Phycology 39: 12-25.

Laemmli UK. 1970. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227: 680-685.

Lin S, Henze S, Lundgren P, Bergman B, Carpenter EJ. 1998. Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Applied and Environmental Microbiology 64: 3052-3058.

Maxwell K, Johnson GN. 2000. Chlorophyll fluorescence - a practical guide. Journal of Experimental Botany 51: 659-668.

Meunier PC, Colón-López MS, Sherman LA. 1997. Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Plant Physiology 115: 991-1000.

Meunier PC, Colón-López MS, Sherman LA. 1998. Photosystem II cyclic heterogeneity and photoactivation in the diazotrophic, unicellular cyanobacterium Cyanothece Species ATCC 51142. Plant Physiology 116: 1551-1562.

Michel KP, Pistorius EK. 2004. Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: the function of IdiA and IsiA. Physiologia Plantarum 120: 36-50.

Milligan AJ, Berman-Frank I, Gerchman Y, Dismukes GC, Falkowski PG. 2007. Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. Journal of Phycology 43: 845-852.

Misra HS, Mahajan SK. 2000. Excitation energy transfer from phycobilisomes to photosystems: a phenomenon associated with the temporal separation of photosynthesis and nitrogen fixation in a cyanobacterium, Plectonema boryanum. Biochimica et Biophysica Acta 1459: 139-147.

Morel FMM, Price NM. 2003. The biogeochemical cycles of trace metals in the oceans. Science 300: 944-647.

Öquist G. 1971. Changes in pigment composition and photosynthesis induced by iron deficiency in the blue-green algae Anacystis nidulans. Physiologia Plantarum 25: 188-191.

Öquist G. 1974a. Iron deficiency in the blue-green algae Anacystis nidulans. Physiologia Plantarum 30: 30-37.

Öquist G. 1974b. Iron deficiency in the blue-green algae Anacystis nidulans: fluorescence and absorption spectra recorded at 77 K. Physiologia Plantarum 31: 55-58.

Paerl HW, Crocker KM, Prufert LE. 1987. Limitation of N2 fixation in coastal marine waters - relative importance of molybdenum, iron, phosphorus, and organic-matter availability. Limnology and Oceanography 32: 525-536.

Postgate JR. 1998. Nitrogen fixation, 3rd edn. Cambridge, UK: Cambridge University Press, 112.

Raven JA, Evans MCW, Korb RE. 1999. The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynthesis Research 60: 111-149.

Rueter JG, Ohki K, Fujita Y. 1990. The effect of iron nutrition on photosynthesis and nitrogen fixation in cultures of Trichodesmium (Cyanophyceae). Journal of Phycology 26: 30-35.

Sandström S, Ivanov AG, Park YI, Öquist G, Gustafsson P. 2003. Iron stress responses in the cyanobacterium Synechococcus sp. PCC 7942. Physiologia Plantarum 116: 255-263.

Sherman LA, Meunier P, Colón-López MS. 1998. Diurnal rhythms in metabolism: a day in the life of a unicellular, diazotrophic cyanobacterium. Physiologia Plantarum 58: 25-42.

Shi T, Sun Y, Falkowski PG. 2007. Effects of iron limitation on the expression of metabolic genes in the marine cyanobacterium Trichodesmium. Environmental Microbiology 9: 2945-2946.

Strasser RJ, Srivastava A, Tsimilli-Michael M. 1999. The fluorescent transient as a tool to characterize and screen photosynthetic samples. In: Mohanty P, Yunus P, eds. Probing photosynthesis: mechanism, regulation and adaptation. London, UK: Taylor and Francis, 445-483.

Subramaniam A, Carpenter EJ, Karentz D, Falkowski PG. 1999. Bio-optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. I. Absorption and action spectra. Limnology and Oceanography 44: 608-617.

Towbin H, Staehlin T, Gordon L. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences, USA 76: 4350-4354.

Tuit C, Waterbury J, Ravizzaz G. 2004. Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria. Limnology and Oceanography 49: 978-990.

Wang WX, Dei RCH. 2003. Bioavailability of iron complexed with organic colloids to the cyanobacteria Synechococcus and Trichodesmium. Aquatic Microbial Ecology 33: 247-259.

Westberry TK, Siegel DA. 2006. Spatial and temporal distribution of Trichodesmium blooms in the world's oceans. Global Biogeochemical Cycles 20, doi 10.1029/2005GB002673.

Yeremenko N, Kouřil R, Ihalainen JA, D’Haene S, Van Oosterwijk N, Andrizhiyevskaya EG, Keegstra W, Dekker HL, Hagemann M, Boekema EJ et al . 2004. Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43: 10308-10313.

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