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Effects of elevated pCO2 on the photosynthetic performance of the sea ice diatoms Navicula directa and Navicula glaciei

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Abstract

Sea ice algal communities are generally dominated by pennate diatoms, which commonly occur at the ice-water interface and in brine channels. They also make a significant contribution to higher trophic levels associated with sea ice habitats. Here, the photosynthetic responses of two sea ice diatom species, Navicula directa and Navicula glaciei, to changes in pCO2 under controlled laboratory conditions were compared. pCO2 (390 ppm and 750 ppm) was manipulated to simulate a shift from present levels (1990) to predicted “IPCC year 2100 worst-case scenario” levels. To investigate these effects, a pulse-amplitude modulation (PAM) fluorometer was used to measure the photosynthetic performance. The ability of the sea ice algae to grow and photosynthesize within physio-chemical gradients in the sea ice suggests that both sea ice species are likely to be well adapted to cope with changes in pCO2 concentrations. Lower pH and higher pCO2 for 7 days resulted in increased biomass, especially for N. directa. However, a decline in photosynthetic capacity (rETRmax) was observed for both species (highest value 11.375 ± 0.163, control; and 8.322 ± 1.282, treatment). Navicula glaciei showed significant effects of elevated pCO2 (p < 0.05) on its photosynthetic response, while N. directa did not. Future changes in CO2 and pH may thus not significantly affect all diatoms but may lead to changes in the photosynthetic activities in some species.

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The data obtained in this study are available from the corresponding author upon request.

References

  • Arrigo KR, Worthen DL, Lizotte MP, Dixon P, Dieckmann G (1997) Primary production in Antarctic sea ice. Science 276:394–397

    Article  CAS  PubMed  Google Scholar 

  • Baragi LV, Khandeparker L, Anil AC (2015) Influence of elevated temperature and pCO2 on the marine periphytic diatom Navicula distans and its associated organisms in culture. Hydrobiologia 762:127–142

    Article  CAS  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 Bio Ecol 406:38–45

    Article  Google Scholar 

  • Consalvey M, Perkins R, Paterson D (2005) PAM fluorescence: a beginners guide for benthic diatomists. Diatom Res 20:1–22

    Article  Google Scholar 

  • Crawfurd KJ, Raven JA, Wheeler GL, Baxter EJ, Joint I (2011) The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PLoS ONE 6:e26695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cummings VJ, Barr NG, Budd RG, Marriott PM, Safi KA, Lohrer AM (2019) In situ response of Antarctic under-ice primary producers to experimentally altered pH. Sci Rep 9:6069

    Article  PubMed  PubMed Central  Google Scholar 

  • Eppley R (1972) Temperature and phytoplankton growth in the sea. Fish Bull 70:1063–1085

    Google Scholar 

  • Falkowski P, Raven J (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton, NJ, USA

  • Feng Y, Warner ME, Zhang Y, Sun J, Fu F-X, Rose JM, Hutchins DA (2008) Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur J Phycol 43:87–98

    Article  CAS  Google Scholar 

  • Feng Y, Chai F, Wells ML, Liao Y, Li P, Cai T, Zhao T, Fu F, Hutchins DA (2021) The combined effects of increased pCO2 and warming on a coastal phytoplankton assemblage: from species composition to sinking rate. Front Mar Sci 8:1–15

  • Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, Raven JA (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. J Plankton Res 32:119–137

    Article  CAS  Google Scholar 

  • Flynn KJK, Blackford JCJ, Baird MME, Raven JA, Clark DR, Beardall JA, Brownlee C, Fabian H, Wheeler GL (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nat Clim Chang 2:760–760

    Article  Google Scholar 

  • Gao K, Campbell DA (2014) Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Funct Plant Biol 41:449–459

    Article  CAS  PubMed  Google Scholar 

  • Garrison D, Gibson A, Coale S, Gowing M, Okolodkov Y, Fritsen CJ, Jeffries M (2005) Sea-ice microbial communities in the Ross Sea: autumn and summer biota. Mar Ecol Prog Ser 300:39–52

    Article  Google Scholar 

  • Genty B, Briantais J-MM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Giordano M, Beardall J, Raven JA (2005) CO2 Concentrating mechanisms in algae : mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies on marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonela confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Hancock AM, Davidson AT, McKinlay J, McMinn A, Schulz KG, van den Enden RL (2018) Ocean acidification changes the structure of an Antarctic coastal protistan community. Biogeosciences 15:2393–2410

    Article  CAS  Google Scholar 

  • Heiden JP, Bischof K, Trimborn S (2016) Light intensity modulates the response of two Antarctic diatom species to ocean acidification. Front Mar Sci 3:1–17

    Article  Google Scholar 

  • Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickland JDH (1965) Fluorometric determination of chlorophyll. Journal du Conseil 30:3–15

    Article  CAS  Google Scholar 

  • Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Natl Acad Sci 108:3830–3837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ihnken S, Robert S, Beardall J (2011) Differential responses of growth and photosynthesis in the marine diatom Chaetoceros muelleri to CO2 and light availability. Phycologia 50:182–193

    Article  CAS  Google Scholar 

  • Jassby AAD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  CAS  Google Scholar 

  • Kang J-S, Kang S-H, Lee JH, Lee S (2002) Seasonal variation of microalgal assemblages at a fixed station in King George Island, Antarctica, 1996. Mar Ecol Prog Ser 229:19–32

    Article  Google Scholar 

  • Kennedy F, McMinn A, Martin A (2012) Effect of temperature on the photosynthetic efficiency and morphotype of Phaeocystis antarctica. J Exp Mar Bio Ecol 429:7–14

    Article  Google Scholar 

  • King AL, Sãudo-Wilhelmy SA, Leblanc K, Hutchins DA, Fu F (2011) CO2 and vitamin B12 interactions determine bioactive trace metal requirements of a subarctic Pacific diatom. ISME J 5:1388–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kvernvik AC, Rokitta SD, Leu E, Harms L, Gabrielsen TM, Rost B, Hoppe CJM (2020) Higher sensitivity towards light stress and ocean acidification in an Arctic sea-ice-associated diatom compared to a pelagic diatom. New Phytol 226:1708–1724

    Article  CAS  PubMed  Google Scholar 

  • Lewis E, Wallace D (1998) Program developed for CO2 system calculations. ORNL/ CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee.

  • Li F, Beardall J, Collins S, Gao K (2017) Decreased photosynthesis and growth with reduced respiration in the model diatom Phaeodactylum tricornutum grown under elevated CO2 over 1800 generations. Glob Chang Biol 23:127–137

    Article  PubMed  Google Scholar 

  • Lizotte MP (2001) The contributions of sea ice algae to Antarctic marine primary production. Am Zool 41:57–73

    Google Scholar 

  • Lizotte MP, Sullivan CW (1992) Photosynthetic capacity in microalgae associated with Antarctic pack ice. Polar Biol 12:497–502

    Article  Google Scholar 

  • Low-Décarie E, Fussmann GF, Bell G (2011) The effect of elevated CO2 on growth and competition in experimental phytoplankton communities. Glob Chang Biol 17:2525–2535

    Article  Google Scholar 

  • Malerba ME, Marshall DJ, Palacios MM, Raven JA, Beardall J (2021) Cell size influences inorganic carbon acquisition in artificially selected phytoplankton. New Phytol 229:2647–2659

    Article  CAS  PubMed  Google Scholar 

  • McCarthy A, Rogers SP, Duffy SJ, Campbell DA (2012) Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta). J Phycol 48:635–646

    Article  CAS  PubMed  Google Scholar 

  • McMinn A, Bleakley N, Steinburner K, Roberts D, Trenerry L (2000) Effect of permanent sea ice cover and different nutrient regimes on the phytoplankton succession of fjords of the Vestfold Hills Oasis, eastern Antarctica. J Plankton Res 22:287–303

    Article  CAS  Google Scholar 

  • McMinn A, Ryan KG, Ralph PJ, Pankowski A (2007) Spring sea ice photosynthesis, primary productivity and biomass distribution in eastern Antarctica, 2002–2004. Mar Biol 151:985–995

    Article  Google Scholar 

  • McMinn A, Martin A, Ryan K (2010) Phytoplankton and sea ice algal biomass and physiology during the transition between winter and spring (McMurdo Sound, Antarctica). Polar Biol 33:1547–1556

    Article  Google Scholar 

  • McMinn A, Müller MN, Martin A, Ryan KG (2014) The response of Antarctic sea ice algae to changes in pH and CO2. PLoS ONE 9:e86984

    Article  PubMed  PubMed Central  Google Scholar 

  • McMinn A, Müller MN, Martin A, Ugalde SC, Lee S, Castrisios K, Ryan KG (2017) Effects of CO2 concentration on a late summer surface sea ice community. Mar Biol 164:1–10

    Article  CAS  Google Scholar 

  • Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998

    Article  CAS  PubMed  Google Scholar 

  • Passow U, Laws EEA (2015) Ocean acidification as one of multiple stressors: Growth response of Thalassiosira weissflogii (diatom) under temperature and light stress. Mar Ecol Prog Ser 541:75–90

    Article  CAS  Google Scholar 

  • Petrou K, Hill R, Brown C (2010) Rapid photoprotection in sea-ice diatoms from the East Antarctic pack ice. Limnol Oceanogr 55:1400–1407

    Article  Google Scholar 

  • Petrou K, Kranz SA, Doblin MA, Ralph PJ (2012) Photophysiological responses of Fragilariopsis cylindrus (Bacillariophyceae) to nitrogen depletion at two temperatures. J Phycol 48:127–136

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Ralph P, McMinn A, Ryan K, Ashworth C (2005) Effect temperature on the photokinetics of microalgae from the surface layers of Antarctic pack ice. J Phycol 41:763–769

    Article  Google Scholar 

  • Richier S, Achterberg EP, Dumousseaud C, Poulton AJ, Suggett DJ, Tyrrell T, Zubkov MV, Moore CM (2014) Carbon cycling and phytoplankton responses within highly replicated shipboard carbonate chemistry manipulation experiments conducted around European shelf seas. Biogeosci Discuss 11:3489-3534

  • Roy RNR, Roy LNL, Vogel KMK, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. Mar Chem 44:249–267

  • Schreiber U, Endo T, Mi H (1995) Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol 36:873–882

    Article  CAS  Google Scholar 

  • Schreiber U (2004) Pulse-Amplitude Modulation (PAM) fluorometry and saturation pulse method. In: Papageorgiou, G & Govindjee [Eds.] Chlorophyll a fluorescence: a signature photosynthesis.. Kluwer, Dordrecht pp, 279–319.

  • Scott P, McMinn A, Hosie G (1994) Physical parameters influencing diatom community structure in eastern Antarctic sea ice. Polar Biol 14:507–517

    Article  Google Scholar 

  • Serôdio J, Vieira S, Cruz S, Coelho H (2007) Rapid light-response curves of chlorophyll fluorescence in microalgae: relationship to steady-state light curves and non-photochemical quenching in benthic diatom-dominated assemblages. Photosynth Res 90:29–43

    Article  Google Scholar 

  • Shi D, Hong H, Su X, Liao L, Chang S, Lin W (2019) The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO2 and pH. J Phycol 55:521–533

    Article  CAS  PubMed  Google Scholar 

  • Stocker TF, Qin D, Plattner GK, et al (2013) Climate change 2013 the physical science basis: Working Group I contribution to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press.

  • Taucher J, Jones J, James A, Brzezinski MA, Carlson CA, Riebesell U, Passow U (2015) Combined effects of CO2 and temperature on carbon uptake and partitioning by the marine diatoms Thalassiosira weissflogii and Dactyliosolen fragilissimus. Limnol Oceanogr 60:901–919

    Article  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 

  • Torstensson A, Hedblom M, Andersson J, Andersson MX, Wulff A (2013) Synergism between elevated pCO2 and temperature on the Antarctic sea ice diatom Nitzschia lecointei. Biogeosciences 10:6391–6401

    Article  CAS  Google Scholar 

  • Torstensson A, Fransson A, Currie K, Wulff A, Chierici M (2018) Microalgal photophysiology and macronutrient distribution in summer sea ice in the Amundsen and Ross Seas, Antarctica. PLoS ONE 13:1–20

    Article  Google Scholar 

  • Trimborn S, Thoms S, Brenneis T, Heiden JP, Beszerti S, Bischof K (2017) Two Southern Ocean diatoms are more sensitive to ocean acidification and changes in irradiance than the Prymnesiophyte Phaeocystis antarctica. Physiol Plant 160:155–170

    Article  CAS  PubMed  Google Scholar 

  • Ugalde SC, Meiners KM, Davidson AT, Westwood KJ, McMinn A (2013) Photosynthetic carbon allocation of an Antarctic sea ice diatom (Fragilariopsis cylindrus). J Exp Mar Biol Ecol 446:228–235

    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 

  • Wu Y, Campbell DA, Irwin AJ, Suggett DJ, Finkel ZV (2014) Ocean acidification enhances the growth rate of larger diatoms. Limnol Oceanogr 59:1027–1034

    Article  CAS  Google Scholar 

  • Zhang Y, Peng C, Wang Z, Zhang J, Li L, Huang S, Li D (2018) The species-specific responses of freshwater diatoms to elevated temperatures are affected by interspecific interactions. Microorganisms 6:82

    Article  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank the Institute of Marine and Antarctic Studies (IMAS), University of Tasmania, for providing the cultures and lab facilities. We are grateful to the following people for their assistance and support in this study: Sarah Ugalde, Lee Shi Hong and Aysha Javeed. The two anonymous reviewers are acknowledged for their constructive comments on the earlier version of this manuscript.

Funding

This research was supported by Yayasan Penyelidikan Sultan Mizan (YPASM) Fellowship Program, MOSTI Flagship Grant (304/CDASAR/650724/P131), and USM Research Grant (1001/PBIOLOGI/8011062 and 1001/CDASAR/8011046).

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SS, AM, and NAMD designed the study and conducted laboratory work, data analysis, and manuscript writing. NAAAM and MM contributed to the data analysis, funding, and writing of the manuscript.

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Correspondence to Sazlina Salleh.

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Salleh, S., Abdul Mubin, N.A.A., Darif, N.A.M. et al. Effects of elevated pCO2 on the photosynthetic performance of the sea ice diatoms Navicula directa and Navicula glaciei. J Appl Phycol 34, 1447–1456 (2022). https://doi.org/10.1007/s10811-022-02709-y

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