The impact of nitrogen deficiency and subsequent recovery on the photosynthetic performance of the red macroalga Gracilariopsis lemaneiformis

  • Xiaojuan Liu
  • Jinyan Wen
  • Canqi Zheng
  • Haojie Jia
  • Weizhou Chen
  • Hong DuEmail author


The effect of nitrogen deficiency and subsequent recovery on photosynthetic performance of the red macroalga Gracilariopsis lemaneiformis was measured in terms of algal growth rate, accumulation of photosynthetic pigments (i.e., phycoerythrin and chlorophyll-a), maximum effective quantum yield of photosystem II (Fv/Fm), and the transcript levels of genes related to photosynthesis and photorespiration. Nitrogen deficiency and then recovery notably promoted the growth of G. lemaneiformis, significantly inhibited the accumulation of phycoerythrin and chlorophyll-a, but had no significant influence on Fv/Fm. In addition to physiological performance of algae under nitrogen stress, the key genes encoding photorespiratory and photosynthetic enzymes (i.e., gdct, gdcp, hpr, shmt, sgat, sbp, and rub) were up-regulated which might have led to more increased in growth rate than that of control after the recovery of nitrogen. While the down-regulation of gdct, gdcp, and shmt genes at the 4th day of nitrogen deficiency might be linked to the reduced accumulation of phycoerythrin and chlorophyll-a, the up-regulation of gdct and gdcp at the beginning of nitrogen deficiency and nitrogen recovery might associate with Fv/Fm that did not change significantly. Briefly, the up- and down-regulation of these genes at different times might be due to an algal complex regulatory mechanism. Thus, the combined action of these genes allows the algae to display higher photosynthetic efficiency and better growth, eventually acclimate to the varying environmental stresses. The data provided here represent a rich source for exploring the function of genes related to photorespiration and photosynthesis as well as the mechanism of algal acclimation under environmental stress.


Gracilariopsis lemaneiformis Rhodophyta N deficiency N recovery Photosynthesis Gene expression 



We thank Dr. Aweya Jude Juventus (a native English speaker) and Muhammad Aslam Buzdar for improving the English.

Authors’ contributions

Hong Du designed and conceived the research. Xiaojuan Liu, Jinyan Wen, Canqi Zheng, Haojie Jia, Weizhou Chen performed the experiments. Hong Du, Xiaojuan Liu, Jinyan Wen, Canqi Zheng, Haojie Jia, Weizhou Chen analyzed the data. Hong Du and Xiaojuan Liu wrote the manuscript.

Funding information

This research was supported by the China Agriculture Research System (CARS-50), International cooperation research project of Shantou University (NC2017001), Start-Up funding of Shantou University (NTF18004), and Department of Education of Guangdong Province (2017KQNCX076).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.


  1. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336CrossRefGoogle Scholar
  2. Borlongan IA, Gerung GS, Kawaguchi S, Nishihara GN, Terada R (2017) Thermal and PAR effects on the photosynthesis of Eucheuma denticulatum and Kappaphycus striatus (so-called Sacol strain) cultivated in shallow bottom of Bali, Indonesia. J Appl Phycol 29:395–404CrossRefGoogle Scholar
  3. Calatrava V, Hom EFY, Llamas Á, Fernández E, Galván A (2018) OK, thanks! A new mutualism between Chlamydomonas and methylobacteria facilitates growth on amino acids and peptides. FEMS Microbiol Lett 365.
  4. Chaloub RM, Motta NMS, de Araujo SP, de Aguiar, da Silva AF (2015) Combined effects of irradiance, temperature and nitrate concentration on phycoerythrin content in the microalga Rhodomonas sp. (Cryptophyceae). Algal Res 8:89–94CrossRefGoogle Scholar
  5. Cosgrove J, Borowitzka M (2011) Chlorophyll fluorescence terminology: an introduction. In: Sugett D, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences. Methods and applications. Springer, Dordrecht, pp 1–17Google Scholar
  6. Cousins AB, Walker BJ, Pracharoenwattana I, Smith SM, Badger MR (2011) Peroxisomal hydroxypyruvate reductase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Photosynth Res 108:91–100CrossRefGoogle Scholar
  7. da Silva AF, Lourenço SO, Chaloub RM (2009) Effects of nitrogen starvation on the photosynthetic physiology of a tropical marine microalga Rhodomonas sp. (Cryptophyceae). Aquat Bot 91:291–297CrossRefGoogle Scholar
  8. Du H, Liang H, Jiang Y, Qu X, Yan H, Liu X (2018) Proteome responses of Gracilaria lemaneiformis exposed to lead stress. Mar Pollut Bull 135:311–317CrossRefGoogle Scholar
  9. Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci 105:17199–17204CrossRefGoogle Scholar
  10. Gómez I, Figueroa FL, Huovinen P, Ulloa N, Morales V (2005) Photosynthesis of the red alga Gracilaria chilensis under natural solar radiation in an estuary in southern Chile. Aquaculture 244:369–382CrossRefGoogle Scholar
  11. Granum E, Roberts K, Raven JA, Leegood RC (2009) Primary carbon and nitrogen metabolic gene expression in the diatom Thalassiosira pseudonana (Bacillariophyceae): diel periodicity and effects of inorganic carbon and nitrogen. J Phycol 45:1083–1092CrossRefGoogle Scholar
  12. Jian J, Zeng D, Wei W, Lin H, Li P, Liu W (2017) The combination of RNA and protein profiling reveals the response to nitrogen depletion in Thalassiosira pseudonana. Sci Rep 7:8989CrossRefGoogle Scholar
  13. Jiang ZJ, Fang JG, Han TT, Mao YZ, Li JQ, Du MR (2014) The role of Gracilaria lemaneiformis in eliminating the dissolved inorganic carbon released from calcification and respiration process of Chlamys farreri. J Appl Phycol 26:545–550CrossRefGoogle Scholar
  14. Kathiresan S, Sarada R, Bhattacharya S, Ravishankar GA (2007) Culture media optimization for growth and phycoerythrin production from Porphyridium purpureum. Biotechnol Bioeng 96:456–463CrossRefGoogle Scholar
  15. Korbee N, Figueroa FL, Aguilera J (2005) Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photochem Photobiol B 80:71–78CrossRefGoogle Scholar
  16. Lewitus AJ, Caron DA (1990) Relative effects of nitrogen or phosphorus depletion on the pigmentation, chemical composition, and volume of Pyrenomonas salina (Cryptophyceae). Mar Ecol Prog Ser 61:171–181CrossRefGoogle Scholar
  17. Liefer JD, Garg A, Campbell DA, Irwin AJ, Finkel ZV (2018) Nitrogen starvation induces distinct photosynthetic responses and recovery dynamics in diatoms and prasinophytes. PLoS One 13:e0195705CrossRefGoogle Scholar
  18. Liu X, Zhang Q, Huan Z, Zhong M, Chen W, Du H (2018) Identification and characterization of glutamine synthetase isozymes in Gracilaria lemaneiformis. Aquat Bot 146:23–30CrossRefGoogle Scholar
  19. Luti S, Caselli A, Taiti C, Bazihizina N, Gonnelli C, Mancuso S, Pazzagli L (2016) PAMP activity of cerato-platanin during plant interaction: an -omic approach. Int J Mol Sci 17:E866CrossRefGoogle Scholar
  20. Martín LA, Rodríguez MC, Matulewicz MC, Fissore EN, Gerschenson LN, Leonardi PI (2013) Seasonal variation in agar composition and properties from Gracilaria gracilis (Gracilariales, Rhodophyta) of the Patagonian coast of Argentina. Phycol Res 61:163–171CrossRefGoogle Scholar
  21. Miller R, Wu G, Deshpande RR, Vieler A, Gärtner K, Li X, Moellering ER, Zäuner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154:1737–1752CrossRefGoogle Scholar
  22. Moreno JI, Martín R, Castresana C (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41:451–463CrossRefGoogle Scholar
  23. Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59CrossRefGoogle Scholar
  24. Nitschke U, Karsten U, Eggert A (2014) Physiological performance of the red alga Stylonema alsidii (Stylonematophyceae) under varying salinities. J Exp Mar Bio Ecol 460:170–176CrossRefGoogle Scholar
  25. Qiao Y, Rong J, Chen H, He C, Wang Q (2015) Non-invasive rapid harvest time determination of oil-producing microalgae cultivations for biodiesel production by using chlorophyll fluorescence. Front Energy Res 3:1–10CrossRefGoogle Scholar
  26. Rai V, Muthuraj M, Gandhi MN, Das D, Srivastava S (2017) Real-time iTRAQ-based proteome profiling revealed the central metabolism involved in nitrogen starvation induced lipid accumulation in microalgae. Sci Rep 7:45732CrossRefGoogle Scholar
  27. Saha SK, Uma L, Subramanian G (2003) Nitrogen stress induced changes in the marine cyanobacterium Oscillatoria willei BDU 130511. FEMS Microbiol Ecol 45:263–272CrossRefGoogle Scholar
  28. Sampath-Wiley P, Neefus CD (2007) An improved method for estimating R-phycoerythrin and R-phycocyanin contents from crude aqueous extracts of Porphyra (Bangiales, Rhodophyta). J Appl Phycol 19:123–129CrossRefGoogle Scholar
  29. Schmidt ÉC, Marthiellen MR, Polo LK et al (2015) Influence of cadmium and salinity in the red alga Pterocladiella capillacea: cell morphology, photosynthetic performance and antioxidant systems. Rev Bras Bot 38:737–749CrossRefGoogle Scholar
  30. Sirikhachornkit A, Suttangkakul A, Vuttipongchaikij S, Juntawong P (2018) De novo transcriptome analysis and gene expression profiling of an oleaginous microalga Scenedesmus acutus TISTR8540 during nitrogen deprivation-induced lipid accumulation. Sci Rep 8:1–12CrossRefGoogle Scholar
  31. Thoisen C, Hansen BW, Nielsen SL (2017) A simple and fast method for extraction and quantification of cryptophyte phycoerythrin. MethodsX 4:209–213CrossRefGoogle Scholar
  32. Timm S, Nunes-Nesi A, Pärnik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20:2848–2859CrossRefGoogle Scholar
  33. Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H (2015) Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. Plant Cell 27:1968–1984CrossRefGoogle Scholar
  34. Valledor L, Furuhashi T, Recuenco-Muñoz L, Wienkoop S, Weckwerth W (2014) System-level network analysis of nitrogen starvation and recovery in Chlamydomonas reinhardtii reveals potential new targets for increased lipid accumulation. Biotechnol Biofuels 7:171CrossRefGoogle Scholar
  35. Vu MTT, Douëtte C, Rayner TA, Thoisen C, Nielsen SL, Hansen BW (2016) Optimization of photosynthesis, growth, and biochemical composition of the microalga Rhodomonas salina—an established diet for live feed copepods in aquaculture. J Appl Phycol 28:1485–1500CrossRefGoogle Scholar
  36. Wang X, Dinler BS, Vignjevic M, Jacobsen S, Wollenweber B (2015) Physiological and proteome studies of responses to heat stress during grain filling in contrasting wheat cultivars. Plant Sci 230:33–50CrossRefGoogle Scholar
  37. Wang J, Sui Z, Hu Y, Zhou W, Wei H, Du Q, Niaz Z, Peng C, Mi P, Que Z (2016a) Assessment of photosynthetic performance, carboxylase activities, and ATP content during tetrasporic development in Gracilariopsis lemaneiformis (Gracilariaceae, Rhodophyta). J Appl Phycol 28:2939–2952CrossRefGoogle Scholar
  38. Wang Y, Feng Y, Wang H, Zhong M, Chen W, Du H (2016b) Physiological and proteomic analyses of two Gracilaria lemaneiformis strains in response to high-temperature stress. J Appl Phycol 28:1847–1858CrossRefGoogle Scholar
  39. Wang X, Xu C, Cai X, Wang Q, Dai S (2017) Heat-responsive photosynthetic and signaling pathways in plants: insight from proteomics. Int J Mol Sci 18:E2191CrossRefGoogle Scholar
  40. Wang Y, Feng Y, Liu X, Zhong M, Chen W, Wang F, Du H (2018) Response of Gracilaria lemaneiformis to nitrogen deprivation. Algal Res 34:82–96CrossRefGoogle Scholar
  41. Wu H (2016, 2016) Effect of different light qualities on growth, pigment content, chlorophyll fluorescence, and antioxidant enzyme activity in the red alga Pyropia haitanensis (Bangiales, Rhodophyta). Biomed Res Int.
  42. Wu J, Zhang Z, Zhang Q, Han X, Gu X, Lu T (2015) The molecular cloning and clarification of a photorespiratory mutant, oscdm1, using enhancer trapping. Front Genet 6:226PubMedPubMedCentralGoogle Scholar
  43. Yang L, Han H, Liu M, Zuo Z, Zhou K, Lü J, Zhu Y, Bai Y, Wang Y (2013) Overexpression of the Arabidopsis photorespiratory pathway gene, serine: Glyoxylate aminotransferase (AtAGT1), leads to salt stress tolerance in transgenic duckweed (Lemna minor). Plant Cell Tissue Organ Cult 113:407–416CrossRefGoogle Scholar
  44. Young EB, Beardall J (2003) Photosynthetic function in Dunaliella tertiolecta (Chlorophyta) during a nitrogen starvation and recovery cycle. J Phycol 39:897–905CrossRefGoogle Scholar
  45. Young EB, Berges JA, Dring MJ (2009) Physiological responses of intertidal marine brown algae to nitrogen deprivation and resupply of nitrate and ammonium. Physiol Plant 135:400–411CrossRefGoogle Scholar
  46. Zhang YM, Chen H, He CL, Wang Q (2013) Nitrogen starvation induced oxidative stress in an oil-producing green alga Chlorella sorokiniana C3. PLoS One 8:69225CrossRefGoogle Scholar
  47. Zhao LS, Su HN, Li K, Xie BB, Liu LN, Zhang XY, Chen XL, Huang F, Zhou BC, Zhang YZ (2016) Supramolecular architecture of photosynthetic membrane in red algae in response to nitrogen starvation. Biochim Biophys Acta Bioenerg 1857:1751–1758CrossRefGoogle Scholar
  48. Zhao LS, Li K, Wang QM, Song XY, Su HN, Xie BB, Zhang XY, Huang F, Chen XL, Zhou BC, Zhang YZ (2017) Nitrogen starvation impacts the photosynthetic performance of Porphyridium cruentum as revealed by chlorophyll a fluorescence. Sci Rep 7:8542CrossRefGoogle Scholar
  49. Zhou W, Sui Z, Wang J, Hu Y, Kang K, Oh J, Kim S, Huang J, Wang P (2014) Biomass and carbon storage of Gracilariopsis lemaneiformis (Rhodophyta) in Zhanshan Bay, Qingdao, China. Chin J Oceanol Limnol 32:1009–1015CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Xiaojuan Liu
    • 1
  • Jinyan Wen
    • 1
  • Canqi Zheng
    • 1
  • Haojie Jia
    • 1
  • Weizhou Chen
    • 1
  • Hong Du
    • 1
    Email author
  1. 1.Guangdong Provincial Key Laboratory of Marine Biotechnology and STU-UNIVPM Joint Algal Research Center, College of SciencesShantou UniversityShantouChina

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