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Population specific responses to temperature and nutrients in the bloom forming Ulva prolifera

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Abstract

Different populations of the same species may have different physiological responses to environmental factors due to the adaptation to their environment. We tested interactive effects of temperatures (10,15, 20, 25, and 30 ℃) and nutrients (low nutrients: 5 μM NO3− and 0.5 μM PO4− (LN); medium nutrients: 50 μM NO3− and 5 μM PO4− (MN); high nutrients: 500 μM NO3− and 50 μM PO4− (HN)) in three different Ulva prolifera strains (one Chinese and two Korean strains). The results showed that all three strains of Ulva survived within the temperature range of 10 to 30 ℃. The photosynthetic rates of all strains increased with increasing temperature from 10 to 30 ℃ under MN. However, at the higher temperature (30 ℃) there was a significant reduction in the photosynthetic rate under HN in all three strains. A positive relationships between tissue nitrogen (N) and chlorophyll or soluble protein were observed in all three strains. The Chinese strain showed the lowest C:N ratio but the highest photosynthetic rate and tissue N contents. Our results show that the bloom forming Chinese strain may have higher nutrient uptake and assimilation ability, leading to higher photosynthetic activity. The Ulva strains may have lower tolerance to higher temperature at high nutrients conditions. These results suggest that the physiological responses of U. prolifera to different temperature and nutrients conditions can be population-specific.

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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Altamirano M, Flores-Moya A, Conde F, Figueroa FL (2000) Growth seasonality, photosynthetic pigments, and carbon and nitrogen content in relation to environmental factors: a field study of Ulva olivascens (Ulvales, Chlorophyta). Phycologia 39:50–58

    Google Scholar 

  • Bao ML, Park JS, Xing QK, He PM, Zhang JH, Yarish C, Yoo HI, Kim JK (2022) Comparative analysis of physiological responses in two Ulva prolifera strains revealed the effect of eutrophication on high temperature and copper stress tolerance. Front Mar Sci 9:863918

    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

    CAS  PubMed  Google Scholar 

  • Berges JA, Varela DE, Harrison PJ (2002) Effects of temperature on growth rate, cell composition and nitrogen metabolism in the marine diatom Thalassiosira pseudonana (Bacillariophyceae). Mar Ecol Prog Ser 225:139–146

    ADS  Google Scholar 

  • Bindoff NL, Cheung WWL, Kairo JG, Arístegui J, Guinder VA, Hallberg R, Hilmi N, Jiao N, Karim MS, Levin L, O’Donoghue S, Purca Cuicapusa SR, Rinkevich B, Suga T, Tagliabue A, Williamson P (2019) Changing ocean, marine ecosystems, and dependent communities. In: Pörtner H-O, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, Mintenbeck K, Alegría A, Nicolai M, Okem A, Petzold J, Rama B, Weyer NM (eds) IPCC special report on the ocean and cryosphere in a changing climate. Cambridge University Press, Cambridge, pp 447–587

  • 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

    CAS  PubMed  Google Scholar 

  • Choi SK, Oh HJ, Yun SH, Lee HJ, Lee K, Han YS, Kim S, Park SR (2020) Population dynamics of the ‘golden tides’ seaweed, Sargassum horneri, on the southwestern coast of Korea: The extent and formation of golden tides. Sustainability 12:2903

    Google Scholar 

  • Coelho C, Marangon J, Rodrigues D, Moura JJG, Romão MJ, Paes de Sousa PM, Correia dos Santos MM (2013) Induced peroxidase activity of haem containing nitrate reductases revealed by protein film electrochemistry. Electroanal Chem 693:105–113

    CAS  Google Scholar 

  • Corey P, Kim JK, Duston J, Garbary DJ, Prithiviraj B (2013) Bioremediation potential of Palmaria palmata and Chondrus crispus (Basin Head): Effect of nitrate and ammonium ratio as nitrogen source on nutrient removal. J Appl Phycol 25:1349–1358

    CAS  Google Scholar 

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

    Google Scholar 

  • Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Google Scholar 

  • Dawes CJ, Koch EW (1990) Physiological responses of the red algae Gracilaria verrucosa and G. tikvahiae before and after nutrient enrichment. Bull Mar Sci 46:335–344

    Google Scholar 

  • Falkowski PG, Raven JA (2013) Aquatic photosynthesis. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Fan X, Xu D, Wang YT, Zhang XW, Cao SN, Mou SL, Ye NH (2014) The effect of nutrients concentrations, nutrients ratios and temperature on photosynthesis and nutrients uptake by Ulva prolifera: implications for the explosion in green tides. J Appl Phycol 26:537–544

    CAS  Google Scholar 

  • Fei X (2012) Solving the coastal eutrophication problem by large scale seaweed. Hydrobiologia 512:145–151

    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

    CAS  PubMed  Google Scholar 

  • Figueira TA, Martins NT, Ayres-Ostrock L, Plastino EM, Enrich-Prast A, de Oliveira VP (2021) The effects of phosphate on physiological responses and carbohydrate production in Ulva fasciata (Chlorophyta) from upwelling and non-upwelling sites. Bot Mar 64:1–11

  • Korbee N (2009) Effects of nutrient supply on photosynthesis and pigmentation in Ulva lactuca (Chlorophyta): Responses to short-term stress. Aquat Biol 7:173-183

  • Gao KS, Xu JT (2008) Effects of solar UV radiation on diurnal photosynthetic performance and growth of Gracilaria lemaneiformis (Rhodophyta). Eur J Phycol 43:297–307

    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

    PubMed  Google Scholar 

  • Gao G, Liu YM, Li XS, Feng ZH, Xu ZG, Wu HY, Xu JT (2017) Expected CO2-induced ocean acidification modulates copper toxicity in the green tide alga Ulva prolifera. Environ Exp Bot 135:63–72

    CAS  Google Scholar 

  • Han HB, Li Y, Ma XJ, Song W, Wang ZL, Fu MZ, Zhang XL (2022) Population differentiation in the dominant species (Ulva prolifera) of green tide in coastal waters of China. Acta Oceanol Sin 41:108–114

    Google Scholar 

  • Han S, Song HI, Park JS, Kim YJ, Umanzor S, Yarish C, Kim JK (2023) Sargassum horneri and Ascophyllum nodosum extracts enhance thermal tolerance and antioxidant activity of Neopyropia yezoensis. J Appl Phycol 35:201-207

  • Hou X, Hou HJ (2013) Roles of manganese in photosystem II dynamics to irradiations and temperatures. Front Biol 8:312–322

    CAS  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

    Google Scholar 

  • Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press, New York, USA

    Google Scholar 

  • Ji Y, Xu ZG, Zou DH, Gao KS (2016) Ecophysiological responses of marine macroalgae to climate change factors. J Appl Phycol 28:2953–2967

    CAS  Google Scholar 

  • Jaime A, Helder TM, Carvalho LF, Esteves E, Rocha C (2014) Macroalgae mitigation potential for fish aquaculture effluents: an approach coupling nitrogen uptake and metabolic pathways using Ulva rigida and Enteromorpha clathrata. Environ Sci Pollut 21:13324–13334

    Google Scholar 

  • Kang JW, Chung IK (2017) The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman. J Appl Phycol 29:2675–2683

    CAS  Google Scholar 

  • Kim JK, Kraemer GP, Neefus CD, Chung IK, Yarish C (2007) Effects of temperature and ammonium on growth, pigment production and nitrogen uptake by four species of Porphyra (Bangiales, Rhodophyta) native to the New England coast. J Appl Phycol 19:431-440

  • Kim JK, Kraemer GP, Yarish C (2008) Physiological activity of Porphyra in relation to zonation. J Exp Mar Biol Ecol 365:75–85

    Google Scholar 

  • Kim JK, Kraemer GP, Yarish C (2009) Research note: comparison of growth and nitrate uptake by New England Porphyra species from different tidal elevations in relation to desiccation. Phycol Res 57:152–157

    CAS  Google Scholar 

  • Kim JK, Kraemer GP, Yarish C (2012) Metabolic plasticity of nitrogen assimilation by Porphyra umbilicalis enables broad intertidal distribution. J Ocean Univ China 11:517–526

    CAS  Google Scholar 

  • Kim JK, Kraemer GP, Yarish C (2013) Effects of emersion on nitrogen release and physiological function in the intertidal genus Porphyra. PLoS One 8:e69961

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Kim JK, Kraemer GP, Yarish C (2015) Use of sugar kelp aquaculture in Long Island Sound and the Bronx River Estuary for nutrient extraction. Mar Ecol Prog Ser 531:155–166

    CAS  ADS  Google Scholar 

  • Kittiwanich J, Yamamoto T, Kawaguchi O, Madinabeitia I (2016) Assessing responses of the Hiroshima Bay ecosystem to increasing or decreasing phosphorus and nitrogen inputs. Mar Pollut Bull 102:256–264

    CAS  PubMed  Google Scholar 

  • Lamb AL, Kim JK, Yarish C, Branco BF (2018) Identification of the bloom forming Ulva and macroalgal assemblage in Jamaica Bay, New York, USA. Rhodora 120:269–299

    Google Scholar 

  • Latimer JS, Tedesco M, Swanson RL, Yarish C, Stacey SP, Garza C (eds) (2014) Long Island sound: prospects for the urban sea. Springer, New York, 558 p

  • Lee JE, Kang JW (2020) The interactive effects of elevated temperature and nutrients concentrations on the physiological responses of Ulva linza Linnaeus (Ulvales, Chlorophyta). J Appl Phycol 32:2459–2467

    CAS  Google Scholar 

  • Li SX, Yu KF, Huo YZ, Zhang JH, Cai WuHL, Ce LYY, Shi DJ, He PM (2016) Effects of nitrogen and phosphorus enrichment on growth and photosynthetic assimilation of carbon in a green tide-forming species (Ulva prolifera) in the Yellow Sea. Hydrobiologia 776:161–171

    CAS  Google Scholar 

  • Li S, Wang P, Zhang C, Zhou X, Yin Z, Hu TY, Hu D, Liu CC, Zhu LD (2020) Influence of polystyrene microplastics on the growth, photosynthetic efficiency and aggregation of freshwater microalgae Chlamydomonas reinhardtii. Sci Total Environ 714:136767

    CAS  PubMed  ADS  Google Scholar 

  • Lohman K, Priscu JC (1992) Physiological indicators of nutrients deficiency in Cladophora (Chlorophyta) in the Clark Fork of the the Columbia river, Montata. J Phycol 28:443–448

    CAS  Google Scholar 

  • Lüning K (1990) Seaweeds: their environment, biogeography, and ecophysiology. John Wiley & Sons Inc., New York

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

    CAS  Google Scholar 

  • Ma C, Qin S, Cui HL, Liu ZY, Zhuang LC, Wang Y, Zhong ZH (2021) Nitrogen enrichment mediates the effects of high temperature on the growth, photosynthesis, and biochemical constituents of Gracilaria blodgettii and Gracilaria lemaneiformis. Environ Sci Pollut Res 28:21256–21265

    CAS  Google Scholar 

  • Martínez B, Arenas F, Rubal M, Burgués S, Esteban R, García-Plazaola I, Figueroa F, Pereira R, Saldaña L, Sousa-Pinto I (2012) Physical factors driving intertidal macroalgae distribution: physiological stress of a dominant fucoid at its southern limit. Oecologia 170:341–353

    PubMed  ADS  Google Scholar 

  • Martins NT (2016) Physiological responses of Ulva fasciata Delile (Ulvales, Chlorophyta): comparison of two populations from thermally distinct sites from Brazilian coast. MSc thesis, Universidade de São Paulo

  • Mawi S, Krishnan S, Din MF, Arumugam N, Chelliapan S (2020) Bioremediation potential of macroalgae Gracilaria edulis and Gracilaria changii co-cultured with shrimp wastewater in an outdoor water recirculation system. Environ Technol Innovat 17:100571

  • Nelson TA, Haberlin K, Nelson AV, Ribarich H, Hotchkiss R, Van Alstyne KL, Buckingham L, Simunds DJ, Fredrickson K (2008) Ecological and physiological controls of species composition in green macroalgal blooms. Ecol 89:1287–1298

    Google Scholar 

  • Ober GT, Thornber CS (2017) Divergent responses in growth and nutritional quality of coastal macroalgae to the combination of increased pCO2 and nutrients. Mar Environ Res 131:69–79

    CAS  PubMed  Google Scholar 

  • Ott FD (1965) Synthetic media and techniques for the xenic cultivation of marine algae and flagellate. Virg J Sci 16:205–218

    CAS  Google Scholar 

  • Park JS, Shin SK, Wu HL, Yarish C, Yoo HI, Kim JK (2021) Evaluation of nutrient bioextraction by seaweed and shellfish aquaculture in Korea. J World Aquacult Soc 52:1118–1134

    CAS  Google Scholar 

  • Polo LK, Felix MR, Kreusch M, Pereira DT, Costa GB, Simioni C, de Paula MR, Latini A, Floh ES, Chow F (2015) Metabolic profile of the brown macroalga Sargassum cymosum (Phaeophyceae, Fucales) under laboratory UV radiation and salinity conditions. J Appl Phycol 27:887–899

    CAS  Google Scholar 

  • Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925

    ADS  Google Scholar 

  • Russell G, Bolton JJ (1975) Euryhaline ecotypes of Ectocarpus siliculosus (Dillw.) Lyngb. Estuar Coast Mar Sci 3:91–94

    ADS  Google Scholar 

  • Reidenbach LB, Fernandez PA, Leal PP, Noisette F, McGraw CM, Revill AT, Hurd CL, Kübler JE (2017) Growth, ammonium metabolism, and photosynthetic properties of Ulva australis (Chlorophyta) under decreasing pH and ammonium enrichment. PLoS One 12:e0188389

    PubMed  PubMed Central  Google Scholar 

  • Ribeiro ALN, Tesima KE, Souza J, Yokoya NS (2013) Effects of nitrogen and phosphorus availabilities on growth, pigment, and protein contents in Hypnea cervicornis J. Agardh (Gigartinales, Rhodophyta). J Appl Phycol 25:1151–1157

    CAS  Google Scholar 

  • Saldarriaga-Hernandez S, Hernandez-Vargas G, Iqbal HMN, Barcelo D, Parra-Saldivar R (2020) Bioremediation potential of Sargassum sp. biomass to tackle pollution in coastal ecosystems: Circular economy approach. Sci Total Environ 715:136978

  • Salo T, Pedersen MF, Boström C (2014) Population specific salinity tolerance in eelgrass (Zostera marina). J Exp Mar Biol Ecol 461:425–429

    CAS  Google Scholar 

  • Samanta P, Shin SK, Jang SJ, Kim JK (2019a) Comparative assessment of salinity tolerance based on physiological and biochemical performances in Ulva australis and Pyropia yezoensis. Algal Res 42:101590

    Google Scholar 

  • Samanta P, Shin SK, Jang SJ, Song YC, Oh S, Kim JK (2019b) Stable carbon and nitrogen isotopic characterization and tracing nutrient sources of Ulva blooms around Jeju coastal areas. Environ Pollut 254:113033

    CAS  PubMed  Google Scholar 

  • Stengel D, Conde-Álvarez R, Connan S, Nitschke U, Arenas F, Abreu H, Barufi JB, Chow F, Robledo D, Malta E (2014) Short-term effects of CO2, nutrients and temperature on three marine macroalgae under solar radiation. Aquat Biol 22:159–176

    Google Scholar 

  • Stocker TF, Qin D, Plattner G-K, Tignor MM, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (2014) Climate change 2013: The physical science basis. In: Contribution of Working Group I to the Fifth Assessment Report of IPCC the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 1535

  • Taylor R, Fletcher R, Raven J (2001) Preliminary studies on the growth of selected ‘green tide’algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Aquat Biol 22:159–176

    Google Scholar 

  • Wang CY, Su RG, Guo LD, Yang B, Zhang Y, Zhang L, Xu H, Shi WJ, Wei LS (2019) Nutrient absorption by Ulva prolifera and the growth mechanism leading to green-tides. Estuar Coast Shelf Sci 227:106329

    CAS  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

  • Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson S (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172

    CAS  PubMed  ADS  Google Scholar 

  • Wiens JJ (2016) Climate-related local extinctions are already widespread among plant and animal species. PLoS Biol 14:e2001104

    PubMed  PubMed Central  Google Scholar 

  • Wu HL, Huo YZ, Zhang JH, Liu YY, Zhang YT, He PM (2015) Bioremediation efficiency of the largest scale artificial Porphyra yezoensis cultivation in the open sea in China. Mar Pollut Bull 95:289–296

    CAS  PubMed  Google Scholar 

  • Wu HL, Kim JK, Huo YZ, Zhang JH, He PM (2017) Nutrient removal ability of seaweeds on Pyropia yezoensis aquaculture rafts in China’s radial sandbanks. Aquat Bot 137:72–79

    Google Scholar 

  • Wu HL, Huo YZ, Yarish C, Kim JK He PM (2018a) Bioremediation and nutrients migration during blooms of Ulva the Yellow Sea, China. Phycologia 57:223-231

  • Wu HL, Shin SK, Jang SJ, Yarish C, Kim JK (2018b) Growth and nutrient bioextraction of Gracilaria chorda, G. vermiculophylla, Ulva prolifera, and U. compressa under hypo- and hyper-osmotic conditions. Algae 33:329–340

    CAS  Google Scholar 

  • Xing QK, Han S, Park JS, Yarish C Kim JK (2023) Comparative transcriptome analysis reveals the molecular mechanism of heat-tolerance in Neopyropia yezoensis induced by Sargassum horneri extract. Front Mar Sci 10:1142483

  • Xu Q, Zhang H, Ju L, Chen M (2014) Interannual variability of Ulva prolifera blooms in the Yellow Sea. Int J Remote Sens 35:4099–4113

    Google Scholar 

  • Ye NH, Zhang XW, Mao YZ, Liang CW, Xu D, Zou J, Zhuang ZM, Wang QY (2011) ‘Green tides’ are overwhelming the coastline of our blue planet: Taking the world’s largest example. Ecol Res 26:477–485

    Google Scholar 

  • Yu Z, Zhu X, Jiang Y, Luo P, Hu C (2014) Bioremediation and fodder potentials of two Sargassum spp. in coastal waters of Shenzhen South China. Mar Pollut Bull 85:797–802

    CAS  PubMed  Google Scholar 

  • Zhang JH, Huo YZ, Yu KF, Chen QF, He Q, Han W, Chen LP, Cao JC, Shi DJ, He PM (2013a) Growth characteristics and reproductive capability of green tide algae in Rudong coast, China. J Appl Phycol 25:795–803

    Google Scholar 

  • Zhang JH, Huo YZ, Zhang ZL, Yu KF, He Q, Zhang LH, Yang LL, Xu R, He PM (2013b) Variations of morphology and photosynthetic performances of Ulva prolifera during the whole green tide blooming process in the Yellow Sea. Mar Environ Res 92:35–42

    CAS  PubMed  Google Scholar 

  • Zou DH, Gao KS (2014) The photosynthetic and respiratory responses to temperature and nitrogen supply in the marine green macroalga Ulva conglobata (Chlorophyta). Phycologia 53:86–94

    CAS  ADS  Google Scholar 

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Funding

This study was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2017R1A6A1A06015181) and by the Ministry of Science and ICT (2022R1A2C1011394), and funded by the Ministry of Oceans and Fisheries of Korea (Project No. 20190518).

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Authors and Affiliations

  1. School of Life Science, Ludong University, Yantai, 264025, China

    Menglin Bao

  2. Department of Marine Science, Incheon National University, Incheon, 22012, Korea

    Menglin Bao & Jang K. Kim

  3. Research Institute of Basic Sciences, Incheon National University, Incheon, 22012, Korea

    Qikun Xing, Ji-Sook Park & Jang K. Kim

  4. College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai, China

    Peimin He & Jianheng Zhang

  5. Department of Ecology and Evolutionary Biology, University of Connecticut, Stamford, CT, 06901, USA

    Charles Yarish

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  1. Menglin Bao
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MB and JK designed the experiment.

MB and JP conducted the experiment.

MB and QX analyzed the data and wrote the first draft of manuscript.

JK provided fund for the experiment and supervised the experiment.

All authors contributed to manuscript revision, read, and approved the submitted version.

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Correspondence to Jang K. Kim.

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Bao, M., Xing, Q., Park, JS. et al. Population specific responses to temperature and nutrients in the bloom forming Ulva prolifera. J Appl Phycol 36, 459–470 (2024). https://doi.org/10.1007/s10811-023-03143-4

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