Skip to main content

Advertisement

SpringerLink
Log in

Effects of seawater acidification on the growth rates of the diatom Thalassiosira (Conticribra) weissflogii under different nutrient, light, and UV radiation regimes

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Effects of ocean acidification (OA) on marine organisms are suggested to be altered by other environmental drivers, such as low nutrient, increased light, and UVR exposures; however, little has been documented on this aspect. Thalassiosira (Conticribra) weissflogii, a marine diatom, was used to examine the OA effects under multiple stressors on its growth. The specific growth rate was inhibited by low nutrient (LN), though it increased with increased sunlight regardless of the nutrient supplies. Presence of UVR reduced the maximal growth rate (μ max) in low CO2 (LC) conditions (both LN and HN) and inhibited the apparent growth light use efficiency (α) in the cells acclimated to LN under both low (LC) and high (HC) CO2 conditions. The HC-grown cells grew faster under HN and low light levels. Conclusively, presence of UVR with high solar radiation, LN and OA acted synergistically to reduce the diatom growth, though, in contrast UVR and OA enhanced the growth under HN.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Reference

  • Beardall J, Young E, Roberts S (2001) Approaches for determining phytoplankton nutrient limitation. Aquat Sci 63:44–69

    Article  CAS  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 

  • Beardall J, Stojkovic S, Gao K (2014) Interactive effects of nutrient supply and other environmental factors on the sensitivity of marine primary producers to ultraviolet radiation: implications for the impacts of global change. Aquat Biol 22:5–23

    Article  Google Scholar 

  • Brennan G, Collins S (2015) Growth responses of a green alga to multiple environmental drivers. Nat Clim Chang 5:892–897

    Article  Google Scholar 

  • Caperon J, Meyer J (1972) Nitrogen-limited growth of marine phytoplankton—I. Changes in population characteristics with steady-state growth rate. Deep Sea Res 19:601–618

    CAS  Google Scholar 

  • Caraco N, Cole J, Likens GE (1990) A comparison of phosphorus immobilization in sediments of freshwater and coastal marine systems. Biogeochemistry 9:277–290

    Article  CAS  Google Scholar 

  • Flynn KJ, Blackford JC, Baird ME, Raven JA, Clark DR, Beardall J, Brownlee C, Fabian H, Wheeler GL (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nat Clim Chang 2:510–513

    Article  CAS  Google Scholar 

  • Flynn KJ, Clark DR, Mitra A, Fabian H, Hansen PJ, Glibert PM, Wheeler GL, Stoecker DK, Blackford JC, Brownlee C (2015) Ocean acidification with (de) eutrophication will alter future phytoplankton growth and succession. Proc R Soc Lond B 282:20142604

    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  Google Scholar 

  • Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993) Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Mar Biol 117:129–132

    Article  CAS  Google Scholar 

  • Gao K, Wu Y, Li G, Wu H, Villafañe VE, Helbling EW (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiol 144:54–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao K, Helbling EW, Häder DP, Hutchins DA (2012a) Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar Ecol Prog Ser 470:167–189

    Article  CAS  Google Scholar 

  • Gao K, Xu J, Gao G, Li Y, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Häder DP, Li W, Xu K, Liu N, Riebesell U (2012b) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nat Clim Chang 2:519–523

    CAS  Google Scholar 

  • Garcia-Gomez C, Gordillo FJ, Palma A, Lorenzo MR, Segovia M (2014) Elevated CO2 alleviates high PAR and UV stress in the unicellular chlorophyte Dunaliella tertiolecta. Photochem Photobiol Sci 13:1347–1358

    Article  CAS  PubMed  Google Scholar 

  • Garside C, Glover HE (1991) Chemiluminescent measurements of nitrate kinetics: I. Thalassiosira pseudonana (clone 3H) and neritic assemblages. J Plankton Res 13:5–19

    CAS  Google Scholar 

  • Gattuso J-P, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. Guide to best practices ocean acidification and data reporting. Publications Office of the European Union, Luxembourg

  • 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 

  • Häder D-P, Gao K (2015) Interactions of anthropogenic stress factors on marine phytoplankton. Front Environ Sci 3:14

    Google Scholar 

  • Häder D-P, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285

    Article  PubMed  Google Scholar 

  • Häder D-P, Williamson CE, Wängberg S-Å, Rautio M, Rose KC, Gao K, Helbling EW, Sinha RP, Worrest R (2015) Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobiol Sci 14:108–126

    Article  PubMed  Google Scholar 

  • Halac SR, Villafane VE, Helbling EW (2010) Temperature benefits the photosynthetic performance of the diatoms Chaetoceros gracilis and Thalassiosira weissflogii when exposed to UVR. J Photochem Photobiol B 101:196–205

    Article  CAS  PubMed  Google Scholar 

  • Hanelt D, Roleda MY (2009) UVB radiation may ameliorate photoinhibition in specific shallow-water tropical marine macrophytes. Aquat Bot 91:6–12

    Article  CAS  Google Scholar 

  • Helbling EW, Zagarese H (eds) (2003) UV effects in aquatic organisms and ecosystems. Royal Society of Chemistry, Cambridge,

    Google Scholar 

  • Helbling EW, Gao K, Gonçalves RJ, Wu H, Villafañe VE (2003) Utilization of solar UV radiation by coastal phytoplankton assemblages off SE China when exposed to fast mixing. Mar Ecol Prog Ser 259:59–66

    Article  CAS  Google Scholar 

  • Hennon GMM, Quay P, Morales RL, Swanson LM, Virginia Armbrust E (2014) Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J Phycol 50:243–253

    Article  CAS  PubMed  Google Scholar 

  • Heraud P, Roberts S, Shelly K, Beardall J (2005) Interactions between UV-B exposure and phosphorus nutrition. II. Effects on rates of damage and repair. J Phycol 41:1212–1218

    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 U S A 108:3830–3837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Chen F, Zhao H, Zeng Z, Chen J (2015) Concentration distribution and structural features of nutrients in the northwest of the South China Sea in winter 2012. J Appl Oceanog 34:310–316

    Google Scholar 

  • Laws EA, Bannister TT (1980) Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnol Oceanog 25:457–473

    Article  CAS  Google Scholar 

  • Laws EA, Pei S, Bienfang P (2013) Phosphate-limited growth of the marine diatom Thalassiosira weissflogii (Bacillariophyceae): evidence of non-monod growth kinetics. J Phycol 49:241–247

    Article  CAS  PubMed  Google Scholar 

  • Li G, Gao K, Gao G (2011) Differential impacts of solar UV radiation on photosynthetic carbon fixation from the coastal to offshore surface waters in the South China Sea. Photochem Photobiol 87:329–334

    Article  CAS  PubMed  Google Scholar 

  • Li W, Gao K, Beardall J (2012a) 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 Y, Gao K, Villafañe V, Helbling E (2012b) Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum. Biogeosciences 9:3931–3942

    Article  CAS  Google Scholar 

  • Li Y, Xu J, Gao K (2014) Light-modulated responses of growth and photosynthetic performance to ocean acidification in the model diatom Phaeodactylum tricornutum. PLoS One 9:e96173

    Article  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 

  • Litchman E, Neale PJ (2005) UV effects on photosynthesis, growth and acclimation of an estuarine diatom and cryptomonad. Mar Ecol Prog Ser 300:53–62

    Article  CAS  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 

  • Meador JA, Baldwin AJ, Catala P, Jeffrey WH, Joux F, Moss JA, Dean Pakulski J, Stevens R, Mitchell DL (2009) Sunlight-induced DNA damage in marine micro-organisms collected along a latitudinal gradient from 70°N to 68°S. Photochem Photobiol 85:412–420

    Article  CAS  PubMed  Google Scholar 

  • Mercado JM, Sobrino C, Neale PJ, Segovia M, Reul A, Amorim AL, Carrillo P, Claquin P, Cabrerizo MJ, León P (2014) Effect of CO2, nutrients and light on coastal plankton. II. Metabolic rates. Aquat Biol 22:43–57

    Article  Google Scholar 

  • Moore JK, Doney SC, Glover DM, Fung IY (2001) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res II 49:463–507

    Article  Google Scholar 

  • Morel FMM, Rueter JG, Anderson DM, Guillard RRL (1979) Aquil: a chemically defined phytoplankton culture medium for trace metal studies. J Phycol 15:135–141

    Article  CAS  Google Scholar 

  • Neale P, Sobrino C, Segovia M, Mercado J, Leon P, Cortés M, Tuite P, Picazo A, Salles S, Cabrerizo M (2014) Effect of CO2, nutrients and light on coastal plankton. I. Abiotic conditions and biological responses. Aquat Biol 22:25–41

    Article  Google Scholar 

  • Passow U, Laws EA (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 

  • Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc Lond B 363:2641–2650

    Article  CAS  Google Scholar 

  • Reul A, Muñoz M, Bautista B, Neale P, Sobrino C, Mercado J, Segovia M, Salles S, Kulk G, León P (2014) Effect of CO2, nutrients and light on coastal plankton. III. Trophic cascade, size structure and composition. Aquat Biol 22:59–76

    Article  Google Scholar 

  • Riebesell U, Tortell PD (2011) Effects of ocean acidification on pelagic organisms and ecosystems. In: Gattuso J-P, Hansson L (eds) Ocean acidification. Oxford University Press, New York, pp. 99–121

    Google Scholar 

  • Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361:249–251

    Article  CAS  Google Scholar 

  • Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367

    Article  CAS  PubMed  Google Scholar 

  • Roberts K, Granum E, Leegood RC, Raven JA (2007) Carbon acquisition by diatoms. Photosynth Res 93:79–88

    Article  CAS  PubMed  Google Scholar 

  • Segovia M, Teresa M, Armando P, García-Gómez C, Lorenzo R, Rivera A, Figueroa FL (2015) Dunaliella tertiolecta (Chlorophyta) avoids cell death under ultraviolet radiation (UVR) by triggering alternative photoprotective mechanisms. Photochem Photobiol 91:1389–1402

    Article  CAS  PubMed  Google Scholar 

  • Shelly K, Heraud P, Beardall J (2002) Nitrogen limitation in Dunaliella tertiolecta (Chlorophyceae) leads to increased susceptibility to damage by ultraviolet-B radiation but also increased repair capacity. J Phycol 38:713–720

    Article  CAS  Google Scholar 

  • Shelly K, Heraud P, Beardall J (2003) Interactive effects of PAR and UV-B radiation on PSII electron transport in the marine alga Dunaliella tertiolecta (Chlorophyceae. J Phycol 39:509–512

    Article  CAS  Google Scholar 

  • Shi D, Kranz SA, Kim JM, Morel FMM (2012) Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc Natl Acad Sci 109:E3094–E3100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith FA, Raven JA (1979) Intracellular pH and its regulation. Annu Rev Plant Physiol 30:289–311

    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 

  • Sobrino C, Segovia M, Neale PJ, Mercado JM, García-Gómez C, Kulk G, Lorenzo MR, Camarena T, van de Poll WH, Spilling K, Ruan Z (2014) Effect of CO2, nutrients and light on coastal plankton. IV. Physiological responses. Aquat Biol 22:77–93

    Article  Google Scholar 

  • Stachura-Suchoples K, Williams DM (2009) Description of Conticribra tricircularis, a new genus and species of Thalassiosirales, with a discussion on its relationship to other continuous cribra species of Thalassiosira Cleve (Bacillariophyta) and its freshwater origin. Eur J Phycol 44:477–486

    Article  Google Scholar 

  • Turley C, Eby M, Ridgwell AJ, Schmidt DN, Findlay HS, Brownlee C, Riebesell U, Fabry VJ, Feely RA, Gattuso J-P (2010) The societal challenge of ocean acidification. Mar Pollut Bull 60:787–792

    Article  CAS  PubMed  Google Scholar 

  • Tyrrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525–531

    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 J, Gao K (2010) Use of UV-A energy for photosynthesis in the red macroalga Gracilaria lemaneiformis. Photochem Photobiol 86:580–585

  • Xu J, Gao K (2012) Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol 160:1762–1769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang G, Gao K (2012) Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity. Mar Environ Res 79:142–151

    Article  PubMed  Google Scholar 

  • Zheng Y, Giordano M, Gao K (2015a) The impact of fluctuating light on the dinoflagellate Prorocentrum micans depends on NO3 − and CO2 availability. J Plant Physiol 180:18–26

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Mario G, Gao K (2015b) Photochemical responses of the diatom Skeletonema costatum grown under elevated CO2 concentration to short-term changes in pH. Aquat Biol 23:109–118

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (41476097; 41430967; 41120164007; 31600317), Natural Science Foundation of Anhui Province (1508085QC67), China Postdoctoral Science Foundation (2015M582039), State Oceanic Administration (National Programme on Global Change and Air-Sea Interaction, GASI-03-01-02-04), doctoral startup project of Huangshan University (2014xkjq002), MEL Visiting Fellowship Program (MELRS1314), and college students’ innovative project of Anhui province (AH2014103753126, 201510375021). W.L. and Y.Y. contributed equally in this study. We thank the two anonymous reviewers for their constructive and valuable comments.

Author information

Authors and Affiliations

  1. College of Life and Environmental Sciences, Huangshan University, Huangshan, 245041, China

    Wei Li & Yuling Yang

  2. State Key Laboratory of Marine Environmental Science/College of Ocean and Earth Sciences, Xiamen University, Xiang-An campus, ZhouLongQuan A1-211, Xiamen, Fujian, 361005, China

    Wei Li, Zhenzhen Li & Kunshan Gao

  3. School of Marine Science and Technology, Huaihai Institute of Technology, Lianyungang, 222005, China

    Zhenzhen Li & Juntian Xu

Authors
  1. Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuling Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhenzhen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juntian Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kunshan Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kunshan Gao.

Additional information

Wei Li and Yuling Yang contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, W., Yang, Y., Li, Z. et al. 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 29, 133–142 (2017). https://doi.org/10.1007/s10811-016-0944-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0944-y

Keywords

Search

Navigation