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Growth and photosynthetic changes of Ulva prolifera in response to diurnal temperature variations

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Abstract

The responses of Ulva species to diurnal temperature difference remain poorly understood. In this present study, we cultured Ulva prolifera under different diurnal temperature treatments with 22°C for photoperiod and 22, 20, 18, 16, 14, and12°C for dark period, respectively (noted as 22-22, 22-20, 22-18, 22-16, 22-14, and 22-12°C treatments). The growth, pigment contents, photosynthesis, superoxide dismutase (SOD) activity, soluble proteins, and sugars were measured. The main results were shown as follows: (1) The growth of U. prolifera was enhanced by the moderate diurnal temperature difference, and the highest growth rate was observed at 22-18°C. (2) Compared with 22-22°C treatment, the thalli grown under 22-18°C condition showed lower chlorophyll a (Chla) content, respiration rate (Rd), the ratio of Rd, and gross photosynthetic rate (Rd/Pg) as well as the net photosynthetic rate (Pn), while the lowest Pn was observed at 22-12°C. (3) The maximum quantum yield (Fv/Fm) was enhanced by diurnal temperature difference, while the effective quantum yield (Fv′/Fm′) decreased with the decreased in temperature in the nighttime. (4) With the increase of the diurnal temperature difference gradient, the SOD activity decreased and then increased, with the lowest value observed at 22-18 °C, and the soluble protein content showed similar trend. Then we cultured this species at 22-22°C and 22-16°C both under 250 and 60 μmol m−2s−1 conditions in order to study the combined effects of diurnal temperature change and light intensities. It was found that under both two light levels, 22-16°C-grown thalli showed higher growth rate, while the SOD activity was lower than that grown under 22-22°C condition. Overall, the suitable range of diurnal temperature difference for the growth of U. prolifera was about 4–6°C and also was mediated by light intensity.

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References

  • Amthor JS, Bar-Even A, Hanson AD, Millar AH, Stitt M, Sweetlove LJ, Tyerman SD (2019) Engineering strategies to boost crop productivity by cutting respiratory carbon loss. Plant Cell 31:297–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao ML, Xing QK, Park JS, He PM, Zhang JH, Yarish C, Kim JK (2023) Temperature and high nutrients enhance hypo-salinity tolerance of the bloom forming green alga, Ulva prolifera. Harmful Algae 123:102402–102402

    Article  CAS  PubMed  Google Scholar 

  • Blomme J, Wichard T, Jacobs TB, De Clerck O (2023) Ulva: an emerging green seaweed model for systems biology. J Phycol 59:433–440

    Article  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Calheiros AC, Sales LPM, Pereira Netto AD, Cavalcanti DN, Castelar B, Reis RP (2021) Commercial raw materials from algaculture and natural stocks of Ulva Spp. J Appl Phycol 33:1805–1818

    Article  CAS  Google Scholar 

  • Chen BB, Xia JR, Zou DH, Zhang X (2019) Responses to ocean acidification and diurnal temperature variation in a commercially farmed seaweed, Pyropia haitanensis (Rhodophyta). Eur J Phycol 54:184–192

    Article  CAS  Google Scholar 

  • Chen YL, Zheng MS, Jiang JN, Hu W, Xu NJ, Li YH (2023) Enhancement of growth in Ulva prolifera by diurnal temperature difference combined with nitrogen enrichment. Mar Environ Res 186:105905

    Article  CAS  PubMed  Google Scholar 

  • Cui JJ, Zhang JH, Huo YZ, Zhou LJ, Wu Q, Chen LP, Yu KF, He PM (2015) Adaptability of free-floating green tide algae in the Yellow Sea to variable temperature and light intensity. Mar Pollut Bull 101:660–666

    Article  CAS  PubMed  Google Scholar 

  • Fan MH, Sun X, Liao Z, Wang JX, Li YH, Xu NJ (2018) Comparative proteomic analysis of Ulva prolifera response to high temperature stress. Proteome Sci 16:17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eggert A (2012) Seaweed responses to temperature. In: Wiencke C, Bischof K (eds) Seaweed Biology. Springer-Verlag, Berlin, Germany, pp 47–66

    Chapter  Google Scholar 

  • Fan MH, Tang XW, Yang ZX, Wang JX, Zhang XL, Yan XJ, Li P, Xu NJ, Liao Z (2022) Integration of the transcriptome and proteome provides insights into the mechanism calcium regulated of Ulva prolifera in response to high-temperature stress. Aquaculture 557:738344

    Article  CAS  Google Scholar 

  • Feng LN, Shi XY, Chen YH, Tang HJ, Wang LS (2021) Effects of temperature on the nitrate reductase activity and growth of Ulva prolifera. J Phycol 57:955–966

    Article  CAS  PubMed  Google Scholar 

  • Fort A, Lebrault M, Allaire M, Esteves-Ferreira AA, McHale M, Lopez F, Farinas-Franco JM, Alseekh S, Fernie AR, Sulpice R (2019) Extensive variations in diurnal growth patterns and metabolism among Ulva spp. strains. Plant Physiol 180:109–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fort A, Mannion C, Farinas-Franco JM, Sulpice R (2020) Green tides select for fast expanding Ulva strains. Sci Total Environ 698:134337

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Gao L, Jiang MJ, Jian A, He LW (2022) The potential of seaweed cultivation to achieve carbon neutrality and mitigate deoxygenation and eutrophication. Environ Res Lett 17:014018

    Article  CAS  Google Scholar 

  • Gao G, Zhong ZH, Zhou XH, Xu JT (2016) Changes in morphological plasticity of Ulva prolifera under different environmental conditions: a laboratory experiment. Harmful Algae 59:51–58

    Article  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases, 1: occurrence in higher plants [Corn, oats, peas]. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo XN, Zhu AN, Chen RS (2021) China’s algal bloom suffocates marine life. Science 373:751

    Article  PubMed  Google Scholar 

  • He YL, Hu CY, Wang YH, Cui DD, Sun X, Li YH, Xu NJ (2018) The metabolic survival strategy of marine macroalga Ulva prolifera under temperature stress. J Appl Phycol 30:3611–3621

    Article  CAS  Google Scholar 

  • He Y, Li MR, Wang YH, Shen SD (2022) The R2R3-MYB transcription factor MYB44 modulates carotenoid biosynthesis in Ulva prolifera. Algal Res 62:102578

    Article  Google Scholar 

  • Hiraoka M, Oka N (2008) Tank cultivation of Ulva prolifera in deep seawater using a new “germling cluster” method. J Appl Phycol 20:97–102

    Article  Google Scholar 

  • Hsu Y-T, Lee T-M (2012) Modulation of gene expression of carotene biosynthesis-related protein by photosynthetic electron transport for the acclimation of intertidal macroalga Ulva fasciata to hypersalinity and excess light. Physiol Plant 144:225–237

    Article  CAS  PubMed  Google Scholar 

  • Huo YZ, Kim JK, Yarish C, Augyte S, He PM (2021) Responses of the germination and growth of Ulva prolifera parthenogametes, the causative species of green tides, to gradients of temperature and light. Aquat Bot 170:103343

    Article  Google Scholar 

  • Jaiswar S, Mungalapara U, Kazi MA, Balar N (2022) Evidence from preliminary experiments revealed drifted Ulva biomass has seedling and aquaculture potential. Aquac Int 30:2833–2846

    Article  CAS  Google Scholar 

  • Jiang H, Gong JY, Lou WY, Zou DH (2019) Photosynthetic behaviors in response to intertidal zone and algal mat density in Ulva lactuca (Chlorophyta) along the coast of Nan’ao Island, Shantou, China. Environ Sci Pollut Res 26:13346–13353

    Article  CAS  Google Scholar 

  • Jiang JN, Yu YY, Zheng MS, Liu NN, Li YH, Xu NJ (2020) High light might alleviate inhibitory effects of high temperature on growth and physiological parameters of Ulva prolifera. Aquac Res 51:2062–2070

    Article  CAS  Google Scholar 

  • Jiang MJ, Gao L, Huang RP, Lin X, Gao G (2022) Differential responses of bloom-forming Ulva intestinalis and economically important Gracilariopsis lemaneiformis to marine heatwaves under changing nitrate conditions. Sci Total Environ 840:156591

    Article  CAS  PubMed  Google Scholar 

  • Keesing JK, Liu D, Fearns P, Garcia R (2011) Inter- and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007-2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China. Mar Pollut Bull 62:1169–1182

    Article  CAS  PubMed  Google Scholar 

  • Li YH, Wang D, Xu XT, Gao XX, Sun X, Xu NJ (2017) Physiological responses of a green algae (Ulva prolifera) exposed to simulated acid rain and decreased salinity. Photosynthetica 55:623–629

    Article  CAS  Google Scholar 

  • Li YH, Zheng MS, Lin JJ, Zhou SD, Sun TC, Xu NJ (2019) Darkness and low nighttime temperature modulate the growth and photosynthetic performance of Ulva prolifera under lower salinity. Mar Pollut Bull 146:85–91

    Article  CAS  PubMed  Google Scholar 

  • Liu DY, Keesing JK, He PM, Wang ZL, Shi YJ, Wang YJ (2013) The world’s largest macroalgal bloom in the Yellow Sea, China: formation and implications. Estuar Coast Shelf Sci 129:2–10

    Article  CAS  Google Scholar 

  • Luo MB, Liu F, Xu ZL (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 

  • McCauley JI, Meyer BJ, Winberg PC, Skropeta D (2016) Parameters affecting the analytical profile of fatty acids in the macroalgal genus Ulva. Food Chem 209:332–340

    Article  CAS  PubMed  Google Scholar 

  • Page TM, Bergstrom E, Diaz-Pulido G (2021) Acclimation history of elevated temperature reduces the tolerance of coralline algae to additional acute thermal stress. Front Mar Sci 8:660196

    Article  Google Scholar 

  • Poor P, Ordog A, Czekus Z, Borbely P, Takacs Z, Kovacs J, Tari I (2018) Regulation of the key antioxidant enzymes by developmental processes and environmental stresses in the dark. Biol Plant 62:201–210

    Article  CAS  Google Scholar 

  • Sillmann J, Kharin VV, Zhang X, Zwiers FW, Bronaugh D (2013) Climate extremes indices in the CMIP5 multimodel ensemble: Part 1. Model evaluation in the present climate. J Geophys Res-Atmos 118:1716–1733

    Article  Google Scholar 

  • Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88

    Article  CAS  PubMed  Google Scholar 

  • Roleda MY, Hurd CL (2019) Seaweed nutrient physiology: application of concepts to aquaculture and bioremediation. Phycologia 58:552–562

    Article  CAS  Google Scholar 

  • Song MJ, Kong FZ, Li YF, Zhao J, Yu RC, Zhou MJ, Jiang P, Yan T (2022) A massive green tide in the Yellow Sea in 2021: field investigation and analysis. Int J Environ Res Public Health 19:11753

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang SY, Huo YZ, Zhang JH, Cui JJ, Wang Y, Yang LL, Zhou QY, Lu YW, Yu KF, He PM (2018) Variations of dominant free-floating Ulva species in the source area for the world’s largest macroalgal blooms, China: differences of ecological tolerance. Harmful Algae 74:58–66

    Article  PubMed  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. Journal of Plant Physiology 144:307–313

  • Wu HL, Chen J, Feng JC, Liu YH, Li XB, Chen R, Xu JT (2022a) Thermal fluctuations and nitrogen enrichment synergistically accelerate biomass yield of Pyropia haitanensis. Aquat Bot 179:103501

    Article  Google Scholar 

  • Wu HL, Liu YM, Beardall J, Zhong ZH, Gao G, Xu JT (2022b) Physiological acclimation of Ulva prolifera to seasonal environmental factors drives green tides in the Yellow Sea. Mar Environ Res 179:105695

    Article  CAS  PubMed  Google Scholar 

  • Wu HL, Zhang JH, Yarish C, He PM, Kim JK (2018) Bioremediation and nutrient migration during blooms of Ulva in the Yellow Sea, China. Phycologia 57(2):223–231

    Article  CAS  Google Scholar 

  • Xu JT, Gao KS (2012) Focus issue on the plant physiology of global change: 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 

  • Yu YY, Lin JJ, Jiang JN, Hu SS, Kang C-K, Xu NJ, Li YH (2022) Environmental history affects the growth and photosynthesis of a green-tide macroalgae Ulva prolifera. Aquac Res 53:2509–2517

    Article  CAS  Google Scholar 

  • Zanolla M, Carmona R, Kawai H, Stengel DB, Altamirano M (2019) Role of thermal photosynthetic plasticity in the dispersal and settlement of two global green tide formers: Ulva pertusa and U. ohnoi. Marine Biology 166:123

    Article  Google Scholar 

  • Zhao H, Liu XH, Jiang T, Cai C, Gu K, Liu YL, He PM (2023a) Activated abscisic acid pathway and C4 pathway, inhibited cell cycle progression, responses of Ulva prolifera to short term high temperature elucidated by multi-omics. Mar Environ Res 183:105796

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Xia ZY, Liu JL, Sun JY, Zhang JH, He PM (2023b) Morphology, growth, and photosynthesis of Ulva prolifera OF Müller (Chlorophyta, Ulvophyceae) gametophytes, the dominant green tide species in the Southern Yellow Sea. J Sea Res 193:102375

    Article  Google Scholar 

  • Zheng MS, Lin JJ, Zhou SD, Zhong JL, Li YH, Xu NJ (2019) Salinity mediates the effects of nitrogen enrichment on the growth, photosynthesis, and biochemical composition of Ulva prolifera. Environ Sci Pollut Res 26:19982–19990

    Article  CAS  Google Scholar 

  • Zheng LX, Wu MQ, Cui YT, Tian L, Yang PS, Zhao LJ, Xue MY, Liu JY (2022) What causes the great green tide disaster in the South Yellow Sea of China in 2021? Ecol Indic 140:108988

    Article  CAS  Google Scholar 

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Funding

This study was supported by the Natural Science Foundation of Zhejiang Province (LY23D060003; LY19D060002) and the Key Program of Science and Technology Innovation in Ningbo (2021Z114, 2023Z118).

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Authors and Affiliations

  1. Key Laboratory of Marine Biotechnology of Zhejiang Province, School of Marine Sciences, Ningbo University, Ningbo, 315211, China

    Wandi Qie, Yanyan Yu, Mingshan Zheng, Jianan Jiang, Nianjun Xu & Yahe Li

  2. Angel Yeast Co., Ltd., Yichang, 443000, China

    Mingshan Zheng

  3. Xiangshan Xuwen Seaweed Development Co. Ltd., Ningbo, 315000, China

    Wenrong Zhu & Yahe Li

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  1. Wandi Qie
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  6. Nianjun Xu
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Contributions

LYH conceived and designed the experiments. QWD, YYY, ZMS and JJN contributed to carry out the experiments. QWD, YYY and ZMS analyzed data. QWD and LYH wrote the paper. QWD, YYY, JJN, ZWR and XNJ revised the manuscript and approved this version for submission. LYH, ZWR and XNJ provided project funding support.

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Correspondence to Yahe Li.

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Qie, W., Yu, Y., Zheng, M. et al. Growth and photosynthetic changes of Ulva prolifera in response to diurnal temperature variations. Aquacult Int (2023). https://doi.org/10.1007/s10499-023-01320-3

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