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.







Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.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.
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.
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.
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.
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.
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.
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.
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.
Doty, M. S. & M. Oguri, 1957. Evidence for a photosynthetic daily periodicity. Limnology and Oceanography 2: 37–40.
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.
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.
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.
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.
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.
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.
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.
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.
Harris, G. P. & B. B. Piccinin, 1977. Photosynthesis by natural phytoplankton populations. Archiv Fur Hydrobiologie 80: 405–457.
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.
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.
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.
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.
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.
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.
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.
Lonergan, T. A., 1984. Regulation of the photosynthetic light reactions by the biological clock. Photochemistry and Photobiology 40: 789–793.
Milton, J. S., 1999. Statistical Methods in the Biological and Health Sciences, 3rd ed. McGraw Hill, Boston, MA.
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.
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.
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.
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.
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.
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.
Portis, A. R., 1995. The regulation of Rubisco by Rubisco activase. Journal of Experimental Botany 46: 1285–1291.
Prezelin, B. B., 1992. Diel periodicity in phytoplankton productivity. Hydrobiologia 238: 1–35.
Prezelin, B. B. & A. C. Ley, 1980. Photosynthesis and chlorophyll-a fluorescence rhythms of marine phytoplankton. Marine Biology 55: 295–307.
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.
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.
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.
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.
Sournia, A., 1974. Circadian periodicities in natural populations of marine phytoplankton. Advances in Marine Biology 12: 325–389.
Stross, R. G., S. W. Chisholm & T. A. Downing, 1973. Causes of daily rhythms in photosynthetic rates of phytoplankton. Biological Bulletin 145: 200–209.
Tabita, F. R., 1988. Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiological Reviews 52: 155–189.
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.
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.
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.
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.
Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-B and pheopigments. Limnology and Oceanography 39: 1985–1992.
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.
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.
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.
Yoshikawa, T. & K. Furuya, 2006. Effects of diurnal variations in phytoplankton photosynthesis obtained from natural fluorescence. Marine Biology 150: 299–311.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Koen Martens
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-011-0862-6


