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Effects of elevated CO2 and nitrogen supply on the growth and photosynthetic physiology of a marine cyanobacterium, Synechococcus sp. PCC7002

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Abstract

Ocean acidification due to increasing atmospheric CO2 concentration and coastal eutrophication are growing global threats to affect marine organisms and ecosystem health. However, little is known about their interactive impacts on marine picocyanobacteria which contribute to a large proportion of primary production. In this study, we cultivated the cyanobacterium Synechococcus sp. PCC7002 at ambient (380 ppmv) and high CO2 (1000 ppmv), across a range of nitrogen levels (LN, 10 μM NO3 ; MN, 35 μM NO3 ; HN, 110 μM NO3 ). In LN media, elevated CO2 significantly decreased cellular chlorophyll a, but insignificantly affected growth rate, photosynthetic efficiency (F v /F m ) and maximum relative electron transport rate (rETRmax). Nitrogen (N)-supply positively increased the growth, F v /F m , dissolved organic carbon (DOC) and cellular carotenoids/Chl a ratios, but decreased the rETRmax in both ambient and elevated CO2 conditions. The cellular C/N ratios were significantly increased by either elevated CO2 or N-supply, and the cell size was significantly enhanced by elevated CO2, not by N-supply. In addition, we found the N-supply alone had no significant effects on the four main components of chromophoric dissolved organic matter (cDOM) in ambient CO2, while the N-supply interacted with elevated CO2 significantly decreasing the cDOM contents in the cultures. Our results indicated that elevated CO2 and N-supply interacted to alter the physiology and cellular biochemistry of Synechococcus sp. PCC7002, providing useful information for understanding the environmental adaptability of Synechococcus to coastal ocean acidification and eutrophication.

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References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polypheno-loxidase in Beta vulgarsis. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beardall J, Sobrino C, Stojkovic S (2009) Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers. Photochem Photobiol Sci 8:1257–1265

    Article  CAS  PubMed  Google Scholar 

  • Beaufort L, Probert I, de Garidel-Thoron T, Bendif EM, Ruiz-Pino D, Metzl N, Goyet C, Noelle B, Coupel P, Grelaud M (2011) Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476:80–83

    Article  CAS  PubMed  Google Scholar 

  • Boelen P, Van De Poll WH, Van Der Strate HJ, Neven IA, Beardall J, Buma AGJ (2011) Neither elevated nor reduced CO2 affects the photophysiological performance of the marine Antarctic diatom Chaetoceros brevis. J Exp Mar Biol Ecol 406:38–45

    Article  Google Scholar 

  • Burkhardt S, Zondervan I, Riebesell U (1999) Effect of CO2 concentration on C:N:P ratio in marine phytoplankton: a species comparison. Limnol Oceanogr 44:683–690

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    Article  CAS  PubMed  Google Scholar 

  • Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Biogeochem Cycl 19:GB2024

  • Chen B, Wang L, Song S, Huang B, Sun J, Liu H (2011) Comparisons of picophytoplankton abundance, size, and fluorescence between summer and winter in northern South China Sea. Cont Shelf Res 31:1527–1540

    Article  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • Endres S, Unger J, Wannicke N, Nausch M, Voss M, Engel A (2013) Response of Nodularia spumigena to pCO2—part 2: exudation and extracellular enzyme activities. Biogeosciences 10:567–582

    Article  Google Scholar 

  • Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WKW, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci U S A 11:9824–9829

    Article  Google Scholar 

  • Fu FX, Warner ME, Zhang Y, Feng Y, Hutchins DA (2007) Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (cyanobacteria). J Phycol 43:485–496

    Article  Google Scholar 

  • Gao K, Zheng Y (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob Chang Biol 16:2388–2398

    Article  Google Scholar 

  • Gao K, Ruan Z, Villafane VE, Gattuso J, Helbling EW (2009) Ocean acidification exacerbates the effect of UV radiation on the calcifying of phytoplankter Emiliania huxleyi. Limnol Oceanogr 54:186–1855

    Article  Google Scholar 

  • Gordillo FJL, Jiménez C, Figueroa FL, Niell FX (1999) Effects of increased atmospheric CO2 and N supply on photosynthesis, growth and cell composition of the cyanobacterium Spirulina platensis (Arthrospira). J Appl Phycol 10:461–469

    Article  Google Scholar 

  • Harvey BP, Gwynn-Jones D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol 3:1016–1030

    Article  PubMed  PubMed Central  Google Scholar 

  • Hipkin CR, Thomas RJ, Syrett PJ (1983) Effects of nitrogen deficiency on nitrate reductase, nitrate assimilation and photosynthesis in unicellular marine algae. Mar Biol 77:101–105

    Article  CAS  Google Scholar 

  • Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Physiol 45:577–607

    Article  CAS  Google Scholar 

  • Hutchins DA, Mulholland MR, Fu FX (2009) Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22:128–145

    Article  Google Scholar 

  • IPCC (2001) Climate change 2001: the scientific basis. Contribution of working group I to the third assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 881

    Google Scholar 

  • Israel A, Hophy M (2002) Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob Chang Biol 8:831–840

    Article  Google Scholar 

  • Israel A, Katz S, Dubinsky Z, Merrill JE, Friedlander M (1999) Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhodophyta). J Appl Phycol 11:447–453

    Article  Google Scholar 

  • Ji Y, Xu Z, Zou D, Gao K (2016) Ecophysiological responses of marine macroalgae to climate change factors. J Appl Phycol 28:2953–2967

    Article  CAS  Google Scholar 

  • Jiao N, Yang Y, Koshikawa H, Watanabe M (2002) Influence of hydrographie conditions on picoplankton distribution in the East China Sea. Aquat Microb Ecol 30:37–48

    Article  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132

    Article  PubMed  Google Scholar 

  • Kranz SA, Levitan O, Richter KU, Prášil O, Berman-Frank I, Rost B (2010) Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant Physiol 154:334–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Gao K, Beardall J (2012) Interactive effects of ocean acidification and nitrogen-limitation on the diatom Phaeodactylum tricornutum. PLoS One 7:e51590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Gao K, Beardall J (2015) Nitrate limitation and ocean acidification interact with UV-B to reduce photosynthetic performance in the diatom Phaeodactylum tricornutum. Biogeosciences 12:2383–2393

    Article  CAS  Google Scholar 

  • Li W, Yang Y, Li Z, Xu J, Gao K (2016) Effects of seawater acidification on the growth rates of the diatom Thalassiosira (Conticribra) weissflogii under different nutrient, light, and UV radiation regimes. J Appl Phycol. doi:10.1007/s10811-016-0944-y:1-10

    Google Scholar 

  • Litchman E, Neale PJ, Banaszak AT (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: Photoprotection and repair. Limnol Oceanogr 47:86–94

    Article  CAS  Google Scholar 

  • Lomas M, Hopkinson B, Losh J, Ryan D, Shi D, Xu Y, Morel FMM (2012) Effect of ocean acidification on cyanobacteria in the subtropical north Atlantic. Aquat Microb Ecol 66:211–222

    Article  Google Scholar 

  • Luciani X, Mounier S, Redon R, Bois A (2009) A simple correction method of inner filter effects affecting FEEM and its application to the PARAFAC decomposition. Chemometr Intell Lab 96:227–238

    Article  CAS  Google Scholar 

  • Ludwig M, Bryant DA (2011) Transcription profiling of the model cyanobacterium Synechococcus sp. strain PCC7002 by NextGen (SOLiD™) Sequencing of cDNA. Front Microbiol 2:41

  • Ludwig M, Bryant DA (2012) Synechococcus sp. strain PCC7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front Microbiol 3:354

  • Mackey KR, Paytan A, Caldeira K, Grossman AR, Moran D, Mcilvin M, Mak AS (2013) Effect of temperature on photosynthesis and growth in marine Synechococcus spp. Plant Physiol 163:815–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marie D, Partensky F, Vaulot D, Brussaard C (1999) Enumeration of phytoplankton, bacteria, and viruses in marine samples. Curr Protocols Cytom 11:1–15

    Google Scholar 

  • Moisan TA, Blattner KL, Makinen CP (2010) Influences of temperature and nutrients on Synechococcus abundance and biomass in the southern Mid-Atlantic Bight. Cont Shelf Res 30:1275–1282

    Article  Google Scholar 

  • Olischläger M, Wiencke C (2013) Ocean acidification alleviates low temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta). J Exp Bot 64:5587–5597

    Article  PubMed  Google Scholar 

  • Partensky F, Blanchot J, Vaulot D (1999) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In: Charpy L, Larkum A (eds) Marine cyanobacteria. Musée Océanographique, Monaco ville, pp 457–475

  • Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Price GD, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461

    Article  CAS  PubMed  Google Scholar 

  • Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci 3:291–315

    Article  Google Scholar 

  • Riebesell U, Tortell PD (2011) Effects of ocean acidification on pelagic organisms and ecosystems. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, NewYork, pp 291–311

    Google Scholar 

  • Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhöfer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zöllner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–549

    Article  CAS  PubMed  Google Scholar 

  • Riegman R, Stolte W, Noordeloos AAM, Slezak D (2000) Nutrient uptake and alkaline phosphatase (EC 3:1:3:1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. J Phycol 36:87–96

    Article  CAS  Google Scholar 

  • Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr 53:494–505

    Article  CAS  Google Scholar 

  • Stedmon CA, Bro R (2008) Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnol Oceanogr Methods 6:572–579

    Article  CAS  Google Scholar 

  • Sunda WG, Cai WJ (2012) Eutrophication induced CO2-acidification of subsurface coastal waters: interactive effects of temperature, salinity, and atmospheric PCO2. Environ Sci Technol 46:10651–10659

    Article  CAS  PubMed  Google Scholar 

  • Torstensson A, Chierici M, Wulff A (2012) The influence of increased temperature and carbon dioxide levels on the benthic/sea ice diatom Navicula directa. Polar Biol 35:205–214

    Article  Google Scholar 

  • Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45:744–750

    Article  CAS  Google Scholar 

  • Trimborn S, Wolf-Gladrow DA, Richter KU, Rost B (2009) The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms. J Exp Marine Biol Ecol 376:26–36

    Article  CAS  Google Scholar 

  • Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20

    Article  CAS  Google Scholar 

  • van de Waal DB, Verschoor AM, Verspagen JMH, van Donk E, Huisman J (2010) Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Front Ecol Environ 8:145–152

    Article  Google Scholar 

  • Wellburn AT (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7:2915–2923

    Article  CAS  Google Scholar 

  • Xu D, Gao ZQ, Li F, Fan X, Zhang XW, Ye NH, Mou SL, Liang CW, Li DM (2012) Detection and quantitation of lipid in the microalga Tetraselmis subcordiformis (Wille) Butcher with BODIPY 505/515 staining. Bioresour Technol 127:386–390

    Article  PubMed  Google Scholar 

  • Xu D, Wang DS, Li B, Fan X, Zhang XW, Ye NH, Wang Y, Mou SL, Zhuang Z (2015) Effects of CO2 and seawater acidification on the early stages of Saccharina japonica development. Environ Sci Technol 49:3548–3556

    Article  CAS  PubMed  Google Scholar 

  • Zheng YQ, Gao KS (2009) Impacts of solar UV radiation on the photosynthesis, growth, and UV-absorbing compounds in Gracilaria lemaneiformis (Rhodophyta) grown at different nitrate concentrations. J Phycol 45:314–323

    Article  CAS  PubMed  Google Scholar 

  • Zou D, Gao K (2014) The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 53:86–94

    Article  CAS  Google Scholar 

  • Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, Not F, Massana R, Ulloa O, Scanlan DJ (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10:147–161

    PubMed  Google Scholar 

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Acknowledgements

We thank Richard B. Rivkin and Yonghui Zeng for their valuable suggestions and help with English. This work was supported by the National Key Research and Development Program of China (2016YFA0601402), China SOA grant associated with task (GASI-03-01-02-05), CNOOC Tianjin Branch (CNOOC-KJ 125 FZDXM 00TJ 001-2014), Key R & D projects in Shandong Province (2015GGF01014), and National Natural Science Foundation of China (41606092, 41606153, 41676156). This study is a contribution to the international IMBER project.

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Correspondence to Yongyu Zhang or Nianzhi Jiao.

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Mou, S., Zhang, Y., Li, G. et al. Effects of elevated CO2 and nitrogen supply on the growth and photosynthetic physiology of a marine cyanobacterium, Synechococcus sp. PCC7002. J Appl Phycol 29, 1755–1763 (2017). https://doi.org/10.1007/s10811-017-1089-3

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