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A day in the life in the dynamic marine environment: how nutrients shape diel patterns of phytoplankton photosynthesis and carbon fixation gene expression in the Mississippi and Orinoco River plumes

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Abstract

This research addresses the hypothesis that environmental conditions affect temporal connectivity between daily transcription of ribulose-1,5 bisphosphate carboxylase/oxygenase (Rubisco) genes and photosynthetic capacity among phytoplankton. From surface samples collected in the Mississippi River plume (MRP) and Orinoco River plume (ORP), we made size-fractionated measurements of Rubisco (rbcL) mRNA from four phytoplankton groups (heterokonts, haptophytes, Synechococcus, and Prochlorococcus) and chlorophyll-normalized photosynthesis–irradiance parameters (including light-saturated photosynthetic rate—P Bmax ), plus nutrient uptake and inorganic carbon. Chlorophyll, photosynthesis, nutrient uptake, and total rbcL mRNA levels were substantially greater in the MRP. Rubisco mRNA and P Bmax exhibited characteristic diel patterns. Regressions with temporally offset data revealed photosynthesis cycles correlated to rbcL mRNA, but with a time lag. This delay was greater in the MRP, and greater among cells >2 μm. At both sites, P Bmax of <2 μm cells exhibited an earlier increase and closer temporal coupling to rbcL mRNA, suggesting carbon fixation is under tighter transcriptional control in picoplankton. The data support our hypothesis such that in the MRP, high productivity and apparent nutrient stress (perhaps including pCO2) resulted in earlier transcription and longer delay to increasing P Bmax among larger phytoplankton. Under stress, larger eukaryotic cells may need longer time to translate adequate Rubisco enzyme because of cellular resource limitation or diversion to nutrient acquisition. In the relatively oligotrophic ORP, phytoplankton may conserve cellular resources by restricting the time for Rubisco translation. These findings provide an interesting glimpse into ways marine algae can modulate the physiology of carbon fixation in response to environmental challenges.

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References

  • Behrenfeld, M. J., O. Prasil, M. Babin & F. Bruyant, 2004. In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis. Journal of Phycology 40: 4–25.

    Article  CAS  Google Scholar 

  • Behrenfeld, M. J., K. H. Halsey & A. J. Milligan, 2008. Evolved physiological responses of phytoplankton to their integrated growth environment. Philosophical Transactions of the Royal Society B – Biological Sciences 363: 2687–2703.

    Article  CAS  Google Scholar 

  • Bronk, D. A., P. M. Glibert, T. C. Malone, S. Banahan & E. Sahlsten, 1998. Inorganic and organic nitrogen cycling in Chesapeake Bay: autotrophic versus heterotrophic processes and relationships to carbon flux. Aquatic Microbial Ecology 15: 177–189.

    Article  Google Scholar 

  • Brunet, C., R. Casotti, V. Vantrepotte & F. Conversano, 2007. Vertical variability and diel dynamics of picophytoplankton in the Strait of Sicily, Mediterranean Sea, in summer. Marine Ecology-Progress Series 346: 15–26.

    Article  CAS  Google Scholar 

  • Bruyant, F., M. Babin, B. Genty, O. Prasil, M. J. Behrenfeld, H. Claustre, A. Bricaud, L. Garczarek, J. Holtzendorff, M. Koblizek, H. Dousova & F. Partensky, 2005. Diel variations in the photosynthetic parameters of Prochlorococcus strain PCC 9511: combined effects of light and cell cycle. Limnology and Oceanography 50: 850–863.

    Article  Google Scholar 

  • Chow, T. J. & F. R. Tabita, 1994. Reciprocal light-dark transcriptional control of nif and rbc expression and light-dependent posttranslational control of nitrogenase activity in Synechococcus sp. strain RF-1. Journal of Bacteriology 176: 6281–6285.

    PubMed  CAS  Google Scholar 

  • Corredor, J. E., B. Wawrik, J. H. Paul, H. Tran, L. Kerkhof, J. M. Lopez, A. Dieppa & O. Cardenas, 2004. Geochemical rate-RNA integrated study: ribulose-1,5-bisphosphate carboxylase/oxygenase gene transcription and photosynthetic capacity of planktonic photoautotrophs. Applied and Environmental Microbiology 70: 5459–5468.

    Article  PubMed  CAS  Google Scholar 

  • Cote, B. & T. Platt, 1983. Day-to-day variations in the spring-summer photosynthetic parameters of coastal marine-phytoplankton. Limnology and Oceanography 28: 320–344.

    Article  CAS  Google Scholar 

  • Doty, M. S. & M. Oguri, 1957. Evidence for a photosynthetic daily periodicity. Limnology and Oceanography 2: 37–40.

    Article  Google Scholar 

  • Dudek, N., M. A. Brzezinski & P. A. Wheeler, 1986. Recovery of ammonium nitrogen by solvent extraction for the determination of relative N15 abundance in regeneration experiments. Marine Chemistry 18: 59–69.

    Article  CAS  Google Scholar 

  • Fuhrman, J. A., R. W. Eppley, A. Hagstrom & F. Azam, 1985. Diel variations in bacterioplankton, phytoplankton, and related parameters in the Southern-California bight. Marine Ecology-Progress Series 27: 9–20.

    Article  Google Scholar 

  • Giordano, M., J. Beardall & J. A. Raven, 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56: 99–131.

    Article  PubMed  CAS  Google Scholar 

  • Glibert, P. M., F. Lipschultz, J. J. Mccarthy & M. A. Altabet, 1982. Isotope dilution models of uptake and remineralization of ammonium by marine plankton. Limnology and Oceanography 27: 639–650.

    Article  CAS  Google Scholar 

  • Halsey, K. H., A. J. Milligan & M. J. Behrenfeld, 2010. Physiological optimization underlies growth rate-independent chlorophyll-specific gross and net primary production. Photosynthesis Research 103: 125–137.

    Article  PubMed  CAS  Google Scholar 

  • Harding, L. W., B. W. Meeson, B. B. Prezelin & B. M. Sweeney, 1981. Diel periodicity of photosynthesis in marine phytoplankton. Marine Biology 61: 95–105.

    Article  Google Scholar 

  • Harding, L. W., B. B. Prezelin, B. M. Sweeney & J. L. Cox, 1982a. Diel oscillations of the photosynthesis–irradiance (P–I) relationship in natural assemblages of phytoplankton. Marine Biology 67: 167–178.

    Article  Google Scholar 

  • Harding, L. W., B. B. Prezelin, B. M. Sweeney & J. L. Cox, 1982b. Primary production as influenced by diel periodicity of phytoplankton photosynthesis. Marine Biology 67: 179–186.

    Article  Google Scholar 

  • Harris, G. P. & B. B. Piccinin, 1977. Photosynthesis by natural phytoplankton populations. Archiv Fur Hydrobiologie 80: 405–457.

    CAS  Google Scholar 

  • Hartman, F. C. & M. R. Harpel, 1994. Structure, function, regulation, and assembly of d-ribulose-1,5-bisphosphatecarboxylase oxygenase. Annual Review of Biochemistry 63: 197–234.

    Article  PubMed  CAS  Google Scholar 

  • John, D. E., S. S. Patterson & J. H. Paul, 2007a. Phytoplankton-group specific quantitative polymerase chain reaction assays for RuBisCO mRNA transcripts in seawater. Marine Biotechnology 9: 747–759.

    Article  PubMed  CAS  Google Scholar 

  • John, D. E., Z. A. Wang, X. W. Liu, R. H. Byrne, J. E. Corredor, J. M. Lopez, A. Cabrera, D. A. Bronk, F. R. Tabita & J. H. Paul, 2007b. Phytoplankton carbon fixation gene (RuBisCO) transcripts and air–sea CO2 flux in the Mississippi River plume. ISME Journal 1: 517–531.

    Article  PubMed  CAS  Google Scholar 

  • John, D. E., B. L. Zielinski, D. A. Bronk, R. H. Byrne, J. E. Corredor & J. H. Paul, 2008. Quantification and Cloning of Carbon-fixation (RuBisCO) mRNA Transcripts from the Orinoco River Plume and Eastern Caribbean Sea, Poster 921. American Society of Limnology and Oceanography (ASLO) Ocean Science Meeting, Orlando, FL, USA.

  • Kana, T. M., J. L. Watts & P. M. Glibert, 1985. Diel periodicity in the photosynthetic capacity of coastal and offshore phytoplankton assemblages. Marine Ecology-Progress Series 25: 131–139.

    Article  Google Scholar 

  • Lavaud, J., R. F. Strzepek & P. G. Kroth, 2007. Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnology and Oceanography 52: 1188–1194.

    Article  CAS  Google Scholar 

  • Legendre, L., S. Demers, C. Garside, E. M. Haugen, D. A. Phinney, L. P. Shapiro, J. C. Therriault & C. M. Yentsch, 1988. Circadian photosynthetic activity of natural marine phytoplankton isolated in a tank. Journal of Plankton Research 10: 1–6.

    Article  Google Scholar 

  • Li, L. A. & F. R. Tabita, 1994. Transcription control of ribulose-bisphosphate carboxylase oxygenase activase and adjacent genes in Anabaena species. Journal of Bacteriology 176: 6697–6706.

    PubMed  CAS  Google Scholar 

  • Lonergan, T. A., 1984. Regulation of the photosynthetic light reactions by the biological clock. Photochemistry and Photobiology 40: 789–793.

    Article  CAS  Google Scholar 

  • Milton, J. S., 1999. Statistical Methods in the Biological and Health Sciences, 3rd ed. McGraw Hill, Boston, MA.

    Google Scholar 

  • Odriozola, A. L., R. Varela, C. Hua, Y. Astor, L. Lorenzoni & F. E. Muller-Karger, 2007. On the absorption of light in the Orinoco River plume. Continental Shelf Research 27: 1447–1464.

    Article  Google Scholar 

  • Paul, J. H., S. L. Pichard, J. B. Kang, G. M. F. Watson & F. R. Tabita, 1999. Evidence for a clade-specific temporal and spatial separation in ribulose bisphosphate carboxylase gene expression in phytoplankton populations off Cape Hatteras and Bermuda. Limnology and Oceanography 44: 12–23.

    Article  Google Scholar 

  • Paul, J. H., J. B. Kang & F. R. Tabita, 2000. Diel patterns of regulation of rbcL transcription in a cyanobacterium and a prymnesiophyte. Marine Biotechnology 2: 429–436.

    PubMed  CAS  Google Scholar 

  • Pichard, S. L., L. Campbell, J. B. Kang, F. R. Tabita & J. H. Paul, 1996. Regulation of ribulose bisphosphate carboxylase gene expression in natural phytoplankton communities 1. Diel rhythms. Marine Ecology-Progress Series 139: 257–265.

    Article  CAS  Google Scholar 

  • Platt, T., S. Sathyendranath & P. Ravindran, 1990. Primary production by phytoplankton – analytic solutions for daily rates per unit area of water-surface. Proceedings of the Royal Society of London Series B – Biological Sciences 241: 101–111.

    Article  Google Scholar 

  • Platt, T., S. Sathyendranath, O. Ulloa, W. G. Harrison, N. Hoepffner & J. Goes, 1992. Nutrient control of phytoplankton photosynthesis in the western North Atlantic. Nature 356: 229–231.

    Article  Google Scholar 

  • Portis, A. R., 1995. The regulation of Rubisco by Rubisco activase. Journal of Experimental Botany 46: 1285–1291.

    CAS  Google Scholar 

  • Prezelin, B. B., 1992. Diel periodicity in phytoplankton productivity. Hydrobiologia 238: 1–35.

    Article  CAS  Google Scholar 

  • Prezelin, B. B. & A. C. Ley, 1980. Photosynthesis and chlorophyll-a fluorescence rhythms of marine phytoplankton. Marine Biology 55: 295–307.

    Article  CAS  Google Scholar 

  • Prezelin, B. B., R. R. Bidigare, H. A. Matlick, M. Putt & B. V. Hoven, 1987. Diurnal patterns of size-fractionated primary productivity across a coastal front. Marine Biology 96: 563–574.

    Article  Google Scholar 

  • Reynolds, A. E., B. L. Mcconaughy & R. A. Cattolico, 1993. Chloroplast genes of the marine alga Heterosigma carterae are transcriptionally regulated during a light/dark cycle. Molecular Marine Biology and Biotechnology 2: 121–128.

    CAS  Google Scholar 

  • Sigman, D. M., K. L. Casciotti, M. Andreani, C. Barford, M. Galanter & J. K. Bohlke, 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Analytical Chemistry 73: 4145–4153.

    Article  PubMed  CAS  Google Scholar 

  • Smith, R. C., B. B. Prezelin, R. R. Bidigare & K. S. Baker, 1989. Biooptical modeling of photosynthetic production in coastal waters. Limnology and Oceanography 34: 1524–1544.

    Article  CAS  Google Scholar 

  • Sournia, A., 1974. Circadian periodicities in natural populations of marine phytoplankton. Advances in Marine Biology 12: 325–389.

    Article  Google Scholar 

  • Stross, R. G., S. W. Chisholm & T. A. Downing, 1973. Causes of daily rhythms in photosynthetic rates of phytoplankton. Biological Bulletin 145: 200–209.

    Article  CAS  Google Scholar 

  • Tabita, F. R., 1988. Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiological Reviews 52: 155–189.

    PubMed  CAS  Google Scholar 

  • Tabita, F. R., 1995. The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. In Blankenship, R. E., M. T. Madigan & C. E. Bauer (eds), Anoxygenic Photosynthetic Bacteria. Kluwer, Dordrecht: 885–914.

    Google Scholar 

  • Tortell, P. D., G. H. Rau & F. M. M. Morel, 2000. Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnology and Oceanography 45: 1485–1500.

    Article  CAS  Google Scholar 

  • Wawrik, B. & J. H. Paul, 2004. Phytoplankton community structure and productivity along the axis of the Mississippi River plume in oligotrophic Gulf of Mexico waters. Aquatic Microbial Ecology 35: 185–196.

    Article  Google Scholar 

  • Wawrik, B., J. H. Paul & F. R. Tabita, 2002. Real-time PCR quantification of rbcL (ribulose-1,5-bisphosphate carboxylase/oxygenase) mRNA in diatoms and pelagophytes. Applied and Environmental Microbiology 68: 3771–3779.

    Article  PubMed  CAS  Google Scholar 

  • Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-B and pheopigments. Limnology and Oceanography 39: 1985–1992.

    Article  CAS  Google Scholar 

  • Wingler, A., P. J. Lea, W. P. Quick & R. C. Leegood, 2000. Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society B – Biological Sciences 355: 1517–1529.

    Article  CAS  Google Scholar 

  • Wyman, M., 1999. Diel rhythms in ribulose-1,5-bisphosphate carboxylase/oxygenase and glutamine synthetase gene expression in a natural population of marine picoplanktonic cyanobacteria (Synechococcus spp.). Applied and Environmental Microbiology 65: 3651–3659.

    PubMed  CAS  Google Scholar 

  • Wyman, M., J. T. Davies, S. Hodgson, G. A. Tarran & D. A. Purdie, 2005. Dynamics of ribulose 1,5-bisphosphate carboxylase/oxygenase gene expression in the coccolithophorid Coccolithus pelagicus during a tracer release experiment in the Northeast Atlantic. Applied and Environmental Microbiology 71: 1659–1661.

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa, T. & K. Furuya, 2006. Effects of diurnal variations in phytoplankton photosynthesis obtained from natural fluorescence. Marine Biology 150: 299–311.

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the U.S. Department of Energy, Office of Science (BER), Grant # DE-FG02-97ER62452. Shiptime in the Gulf of Mexico was made possible by the U.S. National Science Foundation Grant OCE-0221763 to JHP. The authors acknowledge the assistance from the captain and crew of the R/V Pelican (Louisiana Universities Marine Consortium) and additional members of the JHP lab group during cruises. CO2 system data were provided by Zhaohui “Aleck” Wang, Sherwood Liu, and Robert Byrne. MODIS imagery was provided by Remy Luersson of the USF College of Marine Science Institute for Marine Remote Sensing, under direction of Frank Muller-Karger and Chuanmin Hu. The authors also acknowledge the assistance of Chuanmin Hu in compiling the irradiance data.

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Correspondence to David E. John.

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John, D.E., López-Díaz, J.M., Cabrera, A. et al. A day in the life in the dynamic marine environment: how nutrients shape diel patterns of phytoplankton photosynthesis and carbon fixation gene expression in the Mississippi and Orinoco River plumes. Hydrobiologia 679, 155–173 (2012). https://doi.org/10.1007/s10750-011-0862-6

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