Skip to main content
Log in

Rising nutrient nitrogen reverses the impact of temperature on photosynthesis and respiration of a macroalga Caulerpa lentillifera (Ulvophyceae, Caulerpaceae)

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

Abstract

Both temperature and nutrient nitrogen are rising in worldwide aquatic ecosystems. To explore their interactive impacts on algal physiology, we measured the growth, cell components, photosynthesis, and dark respiration of a farmed green alga, Caulerpa lentillifera, under a matrix of temperatures (low, 22 °C; high, 27 °C) and nitrogen concentrations (low, 47 μmol L−1; medium, 188 μmol L−1; high, 750 μmol L−1). The relative growth rate (RGR) was less than 1.0% day−1 at low temperature, which was ~ eightfold higher at high temperature, with no significant effect of nitrogen. Pigment contents of chlorophyll a (Chl a) and carotenoids (Car) and soluble protein content increased with increasing nitrogen levels. High temperature reduced Chl a content under lower nitrogen and enhanced Car contents under higher nitrogen, but had a limited effect on proteins. Photosynthetic parameters, i.e., light-utilized efficiency (α) and maximum photosynthetic rate (Pmax), and dark respiration rate (Rd) increased with increasing nitrogen levels at low temperature. High temperature enhanced the α, Pmax, and Rd under low nitrogen, but reduced them under high nitrogen. Moreover, high temperature lowered both superoxide dismutase (SOD) and catalase (CAT) contents, indicating the beneficial effects on metabolism of C. lentillifera and thus the growth. In addition, our results indicate that the temperature-caused effects on photosynthesis and respiration of C. lentillifera are reversed by increased nitrogen levels.

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

Access this article

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Apiratikul R, Pavasant P (2008) Batch and column studies of biosorption of heavy metals by Caulerpa lentillifera. Bioresour Technol 99:2766–2777

    Article  CAS  PubMed  Google Scholar 

  • Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka MA (2018) The ‘stress’ concept in microalgal biology - homeostasis, acclimation and adaptation. J Appl Phycol 30:2815–2825

  • Chen X, Sun Y, Liu H, Liu S, Qin Y, Li P (2019) Advances in cultivation, wastewater treatment application, bioactive components of Caulerpa lentillifera and their biotechnological applications. Peer J 7:e6118

    Article  PubMed  CAS  Google Scholar 

  • Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2–8

    Article  Google Scholar 

  • Feng Y, Hou L, Ping N, Ling T, Kyo CI (2004) Development of mariculture and its impacts in Chinese coastal waters. Rev Fish Biol Fish 14:1–10

    Article  Google Scholar 

  • Fernandez-Gonzalez C, Perez-Lorenzo M, Pratt N, Moore CM, Bibby TS, Marañón E (2020) Effects of temperature and nutrient supply on resource allocation, photosynthetic strategy, and metabolic rates of Synechococcus sp. J Phycol 56:1–12

    Article  CAS  Google Scholar 

  • Gao X, Choi HG, Park SK, Sun ZM, Nam KW (2019) Assessment of optimal growth conditions for cultivation of the edible Caulerpa okamurae (Caulerpales, Chlorophyta) from Korea. J Appl Phycol 31:1855–1862

    Article  CAS  Google Scholar 

  • Gennaro P, Piazzi L, Persia E, Porrello S (2015) Nutrient exploitation and competition strategies of the invasive seaweed Caulerpa cylindracea. Eur J Phycol 50:384–394

    Article  CAS  Google Scholar 

  • Gordillo FJL, Jiménez C, Goutx M, Niell X (2001) Effects of CO2 and nitrogen supply on the biochemical composition of Ulva rigida with especial emphasis on lipid class analysis. J Plant Physiol 158:367–373

    Article  CAS  Google Scholar 

  • Grosser K, Weissflog I, Dietzek B, Popp J, Pohnert G (2014) Wound plug chemistry and morphology of two species of Caulerpa - a comparative Raman microscopy study. Bot Mar 57:1–7

    Article  CAS  Google Scholar 

  • Guo H, Yao J, Sun Z, Duan D (2015a) Effect of temperature, irradiance on the growth of the green alga Caulerpa lentillifera (Bryopsidophyceae, Chlorophyta). J Appl Phycol 27:879–885

    Article  CAS  Google Scholar 

  • Guo H, Yao J, Sun Z, Duan D (2015b) Effect of salinity and nutrients on the growth and chlorophyll fluorescence of Caulerpa lentillifera. Chin J Oceanol Limnol 33:410–418

    Article  CAS  Google Scholar 

  • Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739

    Article  Google Scholar 

  • Herbeck LS, Unger D (2013) Pond aquaculture effluents traced along back-reef waters by standard water quality parameters, δ15N in suspended matter and phytoplankton bioassays. Mar Ecol Prog Ser 478:71–86

    Article  CAS  Google Scholar 

  • Huang J (2012) Effects of concentrations of nitrogen and phosphorus and different culture methods on the growth of Caulerpa lentillifera. J Fujian Fish 33:–419 (In Chinese with English abstract)

  • Hughes DJ, Varkey D, Doblin MA, Ingleton T, Mcinnes A, Ralph PJ, Dongen-Vogels VV, Suggett DJ (2018) Impact of nitrogen availability upon the electron requirement for carbon fixation in Australian coastal phytoplankton communities. Limnol Oceanogr 63:1891–1910

    Article  CAS  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 

  • Jiang H, Zou D, Lou W, Chen W, Yang Y (2019) Growth and photosynthesis by Gracilariopsis lemaneiformis (Gracilariales, Rhodophyta) in response to different stocking densities along Nan’ao Island coastal waters. Aquaculture 501:279–284

    Article  Google Scholar 

  • Jin D-Q, Lim CS, Sung J-Y, Choi HG, Ha I, Han J-S (2006) Ulva conglobata, a marine alga, has neuroprotective and anti-inflammatory effects in murine hippocampal and microglial cells. Neurosci Lett 402:154–158

    Article  CAS  PubMed  Google Scholar 

  • Kranz SA, Young JN, Hopkinson BM, Goldman JA, Tortell PD, Morel FM (2015) Low temperature reduces the energetic requirement for the CO2 concentrating mechanism in diatoms. New Phytol 205:192–201

    Article  CAS  PubMed  Google Scholar 

  • Kurashima A, Serisawa Y, Kanbayashi T, Toma T, Yokohama Y (2003) Characteristics in photosynthesis of Caulerpa lentillifera J. Agardh and C. racemosa (Forsskal) J. Agardh var. laete-virens (Montagne) Weber-van Bosse with reference to temperature and light intensity. Jpn J Phycol 51:167–172

    Google Scholar 

  • Li R, Liu S, Li Y, Zhang G, Ren J, Zhang J (2014) Nutrient dynamics in tropical rivers, lagoons, and coastal ecosystems of eastern Hainan Island, South China Sea. Biogeosciences 11:481–506

    Article  Google Scholar 

  • Li G, Brown CM, Jeans JA, Donaher NA, McCarthy A, Campbell DA (2015) The nitrogen costs of photosynthesis in a diatom under current and future pCO2. New Phytol 205:533–543

    Article  CAS  PubMed  Google Scholar 

  • Li H, Zhang Y, Chen J, Zheng X, Liu F, Jiao N (2019) Nitrogen uptake and assimilation preferences of the main green tide alga Ulva prolifera in the Yellow Sea, China. J Appl Phycol 31:625–635

    Article  CAS  Google Scholar 

  • Li G, Qin Z, Zhang J, Lin Q, Ni G, Tan Y, Zou D (2020) Algal density mediates the photosynthetic responses of a marine macroalga Ulva conglobata (Chlorophyta) to temperature and pH changes. Algal Res 46:101797

    Article  Google Scholar 

  • Littler MM, Arnold KE (1982) Primary productivity of marine macroalgal functional-form groups from southwestern North America. J Phycol 18:307–311

    Article  Google Scholar 

  • Liu H, Wang F, Wang Q, Dong S, Tian X (2016) A comparative study of the nutrient uptake and growth capacities of seaweeds Caulerpa lentillifera and Gracilaria lichenoides. J Appl Phycol 28:3083–3089

    Article  CAS  Google Scholar 

  • Liu C, Zou D, Yang Y, Chen B, Jiang H (2017) Temperature responses of pigment contents, chlorophyll fluorescence characteristics, and antioxidant defenses in Gracilariopsis lemaneiformis (Gracilariales, Rhodophyta) under different CO2 levels. J Appl Phycol 29:983–991

    Article  CAS  Google Scholar 

  • Luo M, Liu F, Xu Z (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24

    Article  CAS  Google Scholar 

  • Machalek KM, Davison IR, Falkowski PG (1996) Thermal acclimation and photo acclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19:1005–1016

    Article  CAS  Google Scholar 

  • Malta E-J, Ferreira DG, Vergara JJ, Pérez-Lloréns JL (2005) Nitrogen load and irradiance affect morphology, photosynthesis and growth of Caulerpa prolifera (Bryopsidales: Chlorophyta). Mar Ecol Prog Ser 298:101–114

    Article  CAS  Google Scholar 

  • Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80

    Article  CAS  Google Scholar 

  • Menéndez M (2005) Effect of nutrient pulses on photosynthesis of Chaetomorpha linum from a shallow Mediterranean coastal lagoon. Aquat Bot 82:181–192

    Article  CAS  Google Scholar 

  • Menzel D (1988) How do giant plant cells cope with injury? - the wound response in siphonous green algae. Protoplasma 144:73–91

    Article  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Kumara R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039

    Article  CAS  PubMed  Google Scholar 

  • Nagappan T, Vairappan CS (2014) Nutritional and bioactive properties of three edible species of green algae, genus Caulerpa (Caulerpaceae). J Appl Phycol 26:1019–1027

    Article  CAS  Google Scholar 

  • Necchi O (2004) Photosynthetic responses to temperature in tropical lotic macroalgae. Phycol Res 52:140–148

    Article  Google Scholar 

  • Neori A, Chopin T, Troell M, Buschmann AH, Kraemer G, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern aquaculture. Aquaculture 231:361–391

    Article  Google Scholar 

  • Niwano Y, Beppu F, Shimada T, Kyan R, Yasura K, TamakiM NM, Midorikawa Y, Hamada H (2009) Extensive screening for plant foodstuffs in Okinawa, Japan with anti-obese activity on adipocytes in vitro. Plant Food Hum Nutr 64:6–10

    Article  CAS  Google Scholar 

  • Paul NA, Neveux N, Magnusson M, De Nys R (2014) Comparative production and nutritional value of “sea grapes”-the tropical green seaweeds Caulerpa lentillifera and C. racemosa. J Appl Phycol 26:1833–1844

    CAS  Google Scholar 

  • Pimol P, Khanidtha M, Prasert P (2008) Influence of particle size and salinity on adsorption of basic dyes by agricultural waste: dried seagrape (Caulerpa lentillifera). J Environ Sci 20:760–768

    Article  Google Scholar 

  • Reiko MT, Ihara H (2012) Immunostimulatory activity of polysaccharides isolated from Caulerpa lentillifera on macrophage cells. Biosci Biotechnol Biochem 76:501–505

    Article  CAS  Google Scholar 

  • Saito H, Xue C, Yamashiro R, Moromizato S, Itabashi Y (2010) High polyunsaturated fatty acid levels in two subtropical macroalgae, Cladosiphon okamuranus and Caulerpa lentillifera. J Appl Phycol 46:665–673

    Article  CAS  Google Scholar 

  • Sarada B, Prasad MK, Kumar KK, Murthy CVR (2014) Cadmium removal by macro algae Caulerpa fastigiata: characterization, kinetic, isotherm and thermodynamic studies. J Environ Chem Eng 2:1533–1542

    Article  CAS  Google Scholar 

  • Sharma BR, Rhyu DY (2014) Anti-diabetic effects of Caulerpa lentillifera: stimulation of insulin secretion in pancreatic β-cells and enhancement of glucose uptake in adipocytes. Asian Pac J Trop Biomed 4:575–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J (2008) Field survey and culture studies of Caulerpa in Taiwan. Dissertation, National Sun Yat-sen University, Taipei

  • Shiraiwa Y, Miyachi S (1985) Effects of temperature and CO2 concentration on induction of carbonic anhydrase and changes in efficiency of photosynthesis in Chlorella vulgaris 11h. Plant Cell Physiol 26:543–549

    Article  CAS  Google Scholar 

  • Smith SV (1981) Marine macrophytes as a global carbon sink. Science 211:838–840

    Article  CAS  PubMed  Google Scholar 

  • Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Appl Phycol 45:91–99

    Article  CAS  Google Scholar 

  • Su X, Zou X, Zhu J, Huang H, Liu R, Bao S (2017) Effects of light intensity on chlorophyll fluorescence characteristics of Caulerpa lentillifera. J Fish Sci Chin 24:783–790 (In Chinese with English abstract)

    Google Scholar 

  • Sun Y, Liu Y, Ai C, Song S, Chen X (2019) Caulerpa lentillifera polysaccharides enhance the immunostimulatory activity in immunosuppressed mice in correlation with modulating gut microbiota. Food Funct 10:4315–4329

    Article  CAS  PubMed  Google Scholar 

  • Tilzer MM, Dubinsky Z (1987) Effects of temperature and day length on the mass balance of Antarctic phytoplankton. Polar Biol 7:35–42

    Article  Google Scholar 

  • Wang P (2011) Effects of salinity and light intensity on the growth of Caulerpa lentillifera. Mod Agric Sci Technol 24:131–132 (In Chinese with English Abstract)

    Google Scholar 

  • Wang H, Tang X, Jin Y, Meinita MDN, Chi S, Liu T (2017) The research of culture condition for Caulerpa lentillifera. Trans Oceanol Limnol 6:130–136 (In Chinese with English abstract)

    Google Scholar 

  • Wellburn AR (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 

  • Yang Y, Li C, Nie X, Tang D, Chung IK (2004) Development of mariculture and its impacts in Chinese coastal waters. Rev Fish Bio Fisheries 14:1–10

    Article  Google Scholar 

  • Yang Y, Chai Z, Wang Q, Chen W, He Z, Jiang S (2015) Cultivation of seaweed Gracilaria in Chinese coastal waters and its contribution to environmental improvements. Algal Res 9:236–244

    Article  Google Scholar 

  • Ye C, Zhang M, Zhao J, Yang Y, Zuo Y (2013) Photosynthetic response of the macroalga, Gracilaria lemaneiformis (Rhodophyta), to various N and P levels at different temperatures. Int Rev Hydrobiol 98:245–252

    CAS  Google Scholar 

  • Young JN, Goldman JAL, Kranz SA, Tortell PD, Morel FMM (2015) Slow carboxylation of RubisCO constrains the rate of carbon fixation during Antarctic phytoplankton blooms. New Phytol 205:172–181

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Yang Y (2008) Physiological and biochemical response of seaweed Gracilaria lemaneiformis to concentration changes of N and P. J Exp Mar Biol Ecol 367:142–148

    Article  CAS  Google Scholar 

  • Zemke-White WL, Ohno M (1999) World seaweed utilization: an end-of-century summary. J Appl Phycol 11:369–376

    Article  Google Scholar 

  • Zhang L, Cai C, Guo T, Gu J, Xu H, Zhou Y, Wang Y, Liu C, He P (2011) Anti-cancer effects of polysaccharide and phycocyanin from Porphyra yezoensis. J Mar Sci Technol 19:377–382

    Article  CAS  Google Scholar 

  • Zou D, Gao K (2013) Thermal acclimation of respiration and photosynthesis in the marine macroalga Gracilaria lemaneiformis (Gracilariales, Rhodophyta). J Phycol 49:61–68

    Article  PubMed  Google Scholar 

  • Zou D, Gao K, Luo H (2011) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J Phycol 47:87–97

    Article  CAS  PubMed  Google Scholar 

  • Zou D, Liu S, Du H, Xu J (2012) Growth and photosynthesis in seedlings of Hizikia fusiformis (Harvey) Okamura (Sargassaceae, Phaeophyta) cultured at two different temperatures. J Appl Phycol 24:1321–1327

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by the Natural Science Foundation of Guangdong Province of China (2018B030311029, 2019B121202001), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0407), National Natural Science Foundation (41890853, 31741018, 31971498, 41676156), Special Foundation for National Science and Technology Basic Research Program (2018FY100104), and Guangzhou Science and Technology Project (201707010226, 201904010287).

Author information

Authors and Affiliations

Authors

Contributions

Y. Cai, S. Hu, and X. Shi contributed to performing the experiment. G. Li, Y. Cai, and D. Zou contributed to the experimental designs, data analysis, and paper writing. All authors approved this version to be submitted.

Corresponding author

Correspondence to Dinghui Zou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cai, Y., Li, G., Zou, D. et al. Rising nutrient nitrogen reverses the impact of temperature on photosynthesis and respiration of a macroalga Caulerpa lentillifera (Ulvophyceae, Caulerpaceae). J Appl Phycol 33, 1115–1123 (2021). https://doi.org/10.1007/s10811-020-02340-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02340-9

Keywords

Navigation