Skip to main content
Log in

Photosynthetic response of floating Ulva prolifera to diurnal changes of in-situ environments on the sea surface

  • Ecology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

During yellow sea green tide outbreak, the thalli of Ulva prolifera drifted more than 350 km on the sea surface from offshore of Jiangsu Province to Qingdao city, where they were exposed to complex changes of local environments. The purpose of this study is to investigate the response of the thalli to diurnal changes of environments on the sea surface, and a sea surface environment simulator (SSES) was designed to simulate the natural environment of floating U. prolifera mat. A control experiment is designed in the laboratory, which was processed under suitable conditions (20°C for temperature, 72 μmol photons/(m 2 ·s) for light intensity and 30 for salinity), and an in-situ research was conducted to study the photosynthetic responses of floating U. prolifera to diurnal changes of environments. The results show that the photosynthetic efficiency of the thalli decreased gradually with time, and decreased rapidly after 14:00 local time (LT). After exposed to the environment on the sea surface for 6 h, the photosynthetic activity of the thalli decreased significantly. Furthermore, physiological-level and molecular-level experiments revealed that non-photochemical quenching (NPQ), cyclic electron flow (CEF) and energy redistribution between PSI and PSII all played an important role in the strong photosynthetic plasticity of U. prolifera. NPQ is the most important photoprotective responses to environmental changes before 12:00 LT. The results also confirmed that the CEF and energy redistribution between PSI and PSII are the main synergistic effects for the thalli to adapt to the environmental changes when the process NPQ cannot work. And the result can further reveal the reason why U. prolifera can adapt to the living condition of long distance drift on the sea surface. The findings of this research could provide a theoretical basis for explaining outbreaks of the green tide and instructing the management of the problem.

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.

Similar content being viewed by others

References

  • Abdala–Díaz R T, Cabello–Pasini A, Pérez–Rodríguez E, Álvarez R M C, Figueroa F L. 2006. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Marine Biology, 148 (3): 459–465.

    Article  Google Scholar 

  • Allen J F, Bennett J, Steinback K E, Arntzen C J. 1981. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature, 291 (5810): 25–29.

    Article  Google Scholar 

  • Bilger W, Björkman O. 1990. Role of the xanthophyll cycle in photoprotection elucidated by measurements of lightinduced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research, 25 (3): 173–185.

    Article  Google Scholar 

  • Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix J D, Zito F, Forti G. 2002. Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Reports, 3 (3): 280–285.

    Article  Google Scholar 

  • Gao K S, Xu J T. 2008. Effects of solar UV radiation on diurnal photosynthetic performance and growth of Gracilaria lemaneiformis (Rhodophyta). European Journal of Phycology, 43 (3): 297–307.

    Article  Google Scholar 

  • Gao S, Shen S D, Wang G C, Niu J F, Lin A P, Pan G H. 2011. PSI–driven cyclic electron flow allows intertidal macroalgae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant and Cell Physiology, 52 (5): 885–893.

    Article  Google Scholar 

  • Gao S, Wang G C. 2012. The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). Journal of Experimental Botany, 63 (12): 4 349–4 358.

    Article  Google Scholar 

  • Gylle A M, Isaksson D, Ekelund N G A. 2009. Research note: ecotype differentiation in qualitative content of water soluble organic compounds between marine and brackish Fucus vesiculosus L. (Phaeophyceae). Phycological Research, 57 (2): 127–130.

    Article  Google Scholar 

  • Horton P, Ruban A. 2005. Molecular design of the photosystem II light–harvesting antenna: photosynthesis and photoprotection. Journal of Experimental Botany, 56 (411): 365–373.

    Article  Google Scholar 

  • Huang W, Fu P L, Jiang Y J, Zhang J L, Zhang S B, Hu H, Cao K F. 2013. Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest. Tree Physiology, 33 (2): 211–220.

    Article  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J. 2010. Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature, 464 (7292): 1 210–1 213.

    Article  Google Scholar 

  • Joët T, Cournac L, Peltier G, Havaux M. 2002. Cyclic electron flow around photosystem I in C 3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH–dehydrogenase complex. Plant Physiology, 128 (2): 760–769.

    Google Scholar 

  • Kawai Y, Wada A. 2007. Diurnal sea surface temperature variation and its impact on the atmosphere and ocean: a review. Journal of Oceanography, 63 (5): 721–744.

    Article  Google Scholar 

  • Li X P, Björkman O, Shih C, Grossman A R, Rosenquist M, Jansson S, Niyogi K K. 2000. A pigment–binding protein essential for regulation of photosynthetic light harvesting. Nature, 403 (6768): 391–395.

    Article  Google Scholar 

  • Li Z R, Wakao S, Fischer B B, Niyogi K K. 2009. Sensing and responding to excess light. Annual Review of Plant Biology, 60: 239–260.

    Article  Google Scholar 

  • Lin A P, Shen S D, Wang G C, Yi Q Q, Qiao H J, Niu J F, Pan G H. 2011. Comparison of chlorophyll and photosynthesis parameters of floating and attached Ulva prolifera. Journal of Integrative Plant Biology, 53 (1): 25–34.

    Article  Google Scholar 

  • Liu D Y, Keesing J K, Dong Z J, Zhen Y, Di B P, Shi Y J, Fearns P, Shi P. 2010. Recurrence of the world’s largest green–tide in 2009 in Yellow Sea, China: porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms. Marine Pollution Bulletin, 60 (9): 1 423–1 432.

    Article  Google Scholar 

  • Liu F, Pang S J, Chopin T, Gao S Q, Shan T F, Zhao X B, Li J. 2013. Understanding the recurrent large–scale green tide in the Yellow Sea: temporal and spatial correlations between multiple geographical, aquacultural and biological factors. Marine Environmental Research, 83: 38–47.

    Article  Google Scholar 

  • Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real–time quantitative PCR and the 2CT method. Methods, 25 (4): 402–408.

    Article  Google Scholar 

  • Owens T G. 1986. Light–harvesting function in the diatom Phaeodactylum tricornutum II. Distribution of excitation energy between the photosystems. Plant Physiology, 80 (3): 739–746.

    Google Scholar 

  • Pearson G, Kautsky L, Serrão E. 2000. Recent evolution in Baltic Fucus vesiculosus: reduced tolerance to emersion stresses compared to intertidal (North Sea) populations. Marine Ecology Progress Series, 202: 67–79.

    Article  Google Scholar 

  • Peers G, Truong T B, Ostendorf E, Busch A, Elrad D, Grossman A R, Hippler M, Niyogi K K. 2009. An ancient lightharvesting protein is critical for the regulation of algal photosynthesis. Nature, 462 (7272): 518–521.

    Article  Google Scholar 

  • Plouguerné E, Le Lann K, Connan S, Jechoux G, Deslandes E, Stiger–Pouvreau V. 2006. Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquatic Botany, 85 (4): 337–344.

    Article  Google Scholar 

  • Ramus J, Rosenberg G. 1980. Diurnal photosynthetic performance of seaweeds measured under natural conditions. Marine Biology, 56 (1): 21–28.

    Article  Google Scholar 

  • Schreiber U, Gademann R, Ralph P, Larkum A W D. 1997. Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements. Plant and Cell Physiology, 38 (8): 945–951.

    Article  Google Scholar 

  • Schreiber U. 2004. Pulse–amplitude–modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou G C, Govindjee eds. Chlorophyll a Fluorescence. Springer, Dordrecht. p.279–319.

    Book  Google Scholar 

  • Shikanai T. 2007. Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology, 58: 199–217.

    Article  Google Scholar 

  • Sukenik A, Beardall J, Kromkamp J C, Kopecký J, Masojídek J, van Bergeijk S, Gabai S, Shaham E, Yamshon A. 2009. Photosynthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions. Aquatic Microbial Ecology, 56 (2–3): 297–308.

    Article  Google Scholar 

  • Wagner H, Jakob T, Wilhelm C. 2006. Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytologist, 169 (1): 95–108.

    Article  Google Scholar 

  • Wang Y, Wang Y, Zhu L, Zhou B, Tang X X. 2012. Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions. PLoS One, 7 (8): e38245, https://doi.org10.1371/journal. pone.0038245.

    Article  Google Scholar 

  • Wang Z L, Xiao J, Fan S L, Li Y, Liu X Q, Liu D Y. 2015. Who made the world's largest green tide in China?—an integrated study on the initiation and early development of the green tide in Yellow Sea. Limnology and Oceanography, 60 (4): 1 105–1 117.

    Article  Google Scholar 

  • Ye N H, Zhuang Z M, Jin X S, Wang Q Y, Zhang X W, Li D M, Wang H X, Mao Y Z, Jiang Z J, Li B, Xue Z X. 2008. China is on the track tackling Enteromorpha spp. forming green tide. In: Nature Precedings. Nature Publishing Group. 2008.

    Google Scholar 

  • Zhang X W, Ye N H, Mou S L, Xu D, Fan X. 2013. Occurrence of the PsbS and Lhc SR products in the green alga Ulva linza and their correlation with excitation pressure. Plant Physiology and Biochemistry, 70: 336–341.

    Article  Google Scholar 

  • Zhao J, Jiang P, Liu Z Y, Wei W, Lin H Z, Li F C, Wang J F, Song Q. 2013. The yellow sea green tides were dominated by one species, Ulva ( Enteromorpha ) prolifera, from 2007 to 2011. Chinese Science Bulletin, 58 (19): 2 298–2 302.

    Article  Google Scholar 

  • Zhao X Y, Tang X X, Zhang H X, Qu T F, Wang Y. 2016. Photosynthetic adaptation strategy of Ulva prolifera floating on the sea surface to environmental changes. Plant Physiology and Biochemistry, 107: 116–125.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ying Wang.

Additional information

Supported by the National Key R&D Program of China (No. 2016YFC1402102), the National Natural Science Foundation of China (No. 41706121), the Basic Applied Researching Projects of Qingdao (No. 15-9-1-37-jch), the Fundamental Research Funds for the Central Universities (No. 201513046), the China Postdoctoral Science Foundation (No. 2013M531648), the Natural Science Foundation of Shandong Province (No. ZR2014DP008), and the NSFC-Shandong Joint Fund for Marine Ecology and Environmental Sciences (No. U1606404)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, X., Tang, X., Hu, S. et al. Photosynthetic response of floating Ulva prolifera to diurnal changes of in-situ environments on the sea surface. J. Ocean. Limnol. 37, 589–599 (2019). https://doi.org/10.1007/s00343-019-8081-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-019-8081-5

Keyword

Navigation