Light absorption and impacts of low salinities on photosynthetic behaviour in the epiphytic alga Neosiphonia savatieri (Rhodomelaceae, Rhodophyta)

Abstract

Filamentous epiphyte outbreaks, a serious problem in the commercial cultivation of Kappaphycus/Eucheuma, are often triggered by large changes in abiotic factors. However, the physiological characteristics of epiphytes are poorly understood. In this study, the main pigment contents of Neosiphonia savatieri and its healthy host strains, including green thalli of Kappaphycus striatum (G-KS), brown and green thalli of Kappaphycus alvarezii (B-KA, G-KA), were quantified. The light absorption capacities of lipid- and water-soluble pigments of these seaweeds were also measured. Photosynthetic parameters, including pigment content and fast chlorophyll a fluorescence kinetics, were further studied in N. savatieri exposed to different salinities (16–34 psu) for 10 h in an outdoor experiment. The phycobiliprotein (PBP), Chl-a, and carotenoid contents of N. savatieri were comparatively higher than the hosts, with the values of 2.50, 0.29, and 0.12 mg g−1 (fw), respectively. The mean extinction coefficients of lipid- and water-soluble pigments in N. savatieri were both higher than G-KS, B-KA, and G-KA in the 400–700 nm bands. Salinity of 28 psu increased the pigment contents of the epiphyte, and 16–22 psu did not have a negative impact. Polyphasic fluorescence transients revealed that salinities at 22–28 psu were beneficial to photosynthetic electron transport, mainly attributed to the enhancement of energy absorption per active PSII reaction centre. Given these observations, N. savatieri has a higher light-harvesting capacity and better tolerance to low salinities. These two physiological properties made N. savatieri well suited to the low light and hypo-saline conditions that are frequently triggered by fluctuations in abiotic factors.

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References

  1. Arnon DI (1949) Copper enzymes in isolated chloroplasts phenoloxidases in Beta vulgaris. Plant Physiol 24:1–15

  2. Ask EI (2001) Creating sustainable commercial Eucheuma cultivation industry: the importance and necessity of human factor. In: Chapman ARO, Anderson RJ, Vreeland VJ, Davison IR (eds) Proceedings of the 17th International Seaweed Symposium, Cape Town, pp 13–18

  3. Baghel RS, Reddy CRK, Jha B (2014) Characterization of agarophytic seaweeds from the biorefinery context. Bioresour Technol 159:280–285

    CAS  Article  PubMed  Google Scholar 

  4. Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335

    Article  Google Scholar 

  5. Borlongan IA, Tibubos KR, Yunque DAT, Hurtado AQ, Critchley AT (2011) Impact of AMPEP on the growth and occurrence of epiphytic Neosiphonia infestation on two varieties of commercially cultivated Kappaphycus alvarezii grown at different depths in the Philippines. J Appl Phycol 23:615–621

    Article  Google Scholar 

  6. Borlongan IAG, Luhan MRJ, Padilla PIP, Hurtado AQ (2016) Photosynthetic responses of ‘Neosiphonia sp. epiphyte-infected’ and healthy Kappaphycus alvarezii (Rhodophyta) to irradiance, salinity and pH variations. J Appl Phycol 28:2891–2902

    CAS  Article  Google Scholar 

  7. Crabbe MJ (2009) Climate change and tropical marine agriculture. J Exp Bot 60:2839–2844

    CAS  Article  PubMed  Google Scholar 

  8. Critchley AT, Largo D, Wee W, Bleicher L’honneur G, Hurtado AQ, Schubert J (2004) A preliminary summary on Kappaphycus farming and the impact of epiphytes. Jap J Phycol (Supplement) 52:231–232

    Google Scholar 

  9. Dawes CJ, Orduna-Rojas J, Robledo D (1999) Response of the tropical red seaweed Gracilaria cornea to temperature, salinity and irradiance. J Appl Phycol 10:419–425

  10. Doty MS, Alvarez VB (1975) Status, problem, advances and economics of Eucheuma farms. Mar Technol Soc J 9:30–35

    Google Scholar 

  11. Enríquez S (2003) Light absorption efficiency and the package effect in the leaves of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 49:141–150

    Google Scholar 

  12. Fan X, Xu NJ, Shi JG (2003) Bromophenols from the red alga Rhodomela confervoides. J Nat Prod 66:455–458

    CAS  Article  PubMed  Google Scholar 

  13. Hayashi L, Faria GSM, Nunes BG, Zitta CS, Scariot LA, Rover T, Felix MRL, Bouzon Z (2011) Effects of salinity on the growth rate, carrageenan yield, and cellular structure of Kappaphycus alvarezii (Rhodophyta, Gigartinales) cultured in vitro. J Appl Phycol 23:439–447

    Article  Google Scholar 

  14. Huang Y, Liu JG, Pang T, Li J, Lin W (2010) The changes of primary photochemical reactions in Kappaphycus alvarezii exposed to low salinity. Acta Oceanol Sinica 32:146–152

    CAS  Google Scholar 

  15. Hurtado AQ, Critchley AT, Trespoey A, Lhonneur GB (2006) Occurrence of Polysiphonia epiphytes in Kappaphycus farms at Calaguas Is., Camarines Norte Phillippines. J Appl Phycol 18:301–306

    Article  Google Scholar 

  16. Hurtado AQ, Gerung GS, Yasir S, Critchley AT (2014) Cultivation of tropical red seaweeds in the BIMP-EAGA region. J Appl Phycol 26:707–718

    Article  Google Scholar 

  17. Jensen A (1978) Chlorophylls and carotenoids. In: Hellebust J, Craigie JS (eds) Handbook of phycological methods: physiological and biochemical methods. Cambridge University Press, Cambridge, pp 61–64

    Google Scholar 

  18. Kim MS (2005) Taxonomy of a poorly documented alga, Neosiphonia savatieri (Rhodomelaceae, Rhodophyta) from Korea. Nova Hedwigia 81:163–176

    Article  Google Scholar 

  19. Kumar M, Kumari P, Gupta V, Reddy CRK, Jha B (2010) Biochemical responses of red alga Gracilaria corticata (Gracilariales, Rhodophyta) to salinity induced oxidative stress. J Exp Mar Biol Ecol 391:27–34

    CAS  Article  Google Scholar 

  20. Largo DB, Fukami K, Nishijima T (1995) Occasional bacteria promoting ice-ice disease in the carrageenan-producing red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 7:545–554

    Article  Google Scholar 

  21. Li YF, Meng FP (2014) Type selection of transparent plate for microalgae photo-bioreactor building based on light transmissivity analysis. Acta Opt Sin 1:0123003–0123006

    Google Scholar 

  22. Li YF, Liu JG, Zhang LT, Pang T (2016) Changes of photosynthetic performances in mature thalli of the red alga Gelidium amansii (Gelidiaceae) exposed to different salinities. Mar Biol Res 12:631–639

    Article  Google Scholar 

  23. Macler BA (1988) Salinity effects on photosynthesis, carbon allocation, and nitrogen assimilation in the red alga, Gelidium coulteri. Plant Physiol 88:690–694

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Marinho-Soriano E (2012) Effect of depth on growth and pigment contents of the macroalgae Gracilaria bursa-pastoris. Rev Bras Farmacogn 22:730–735

    CAS  Article  Google Scholar 

  25. Masuda M, Abe T, Kawaguchi S, Phang SM (2001) Taxonomic notes on marine algae from Malaysia VI. Five species of Ceramiales (Rhodophyceae). Bot Mar 44:467–477

    Google Scholar 

  26. Menzel L, Burger G (2002) Climate change scenarios and runoff response in the Mulde catchment (southern Elbe, Germany). J Hydrol 267:53–64

    Article  Google Scholar 

  27. Msuya FE, Buriyo A, Omar I, Pascal B, Narrain K, Ravina JJM, Mrabu E, Wakibia JG (2014) Cultivation and utilisation of red seaweeds in the Western Indian Ocean (WIO) Region. J Appl Phycol 26:699–705

    CAS  Article  Google Scholar 

  28. Mtolera MSP, Collen J, Pedersen M, Ekdahl A, Abrahamsson K, Semesi AK (1996) Stress-induced production of volatile halogenated organic compounds in Eucheuma denticulatum (Rhodophyta) caused by elevated pH and high light intensities. Eur J Phycol 3:89–95

    Article  Google Scholar 

  29. Muzik I (2002) A first-order analysis of the climate change effect on the flood frequencies in a sub-alpine watershed by means of a hydrological rainfall-runoff model. J Hydrol 267:65–73

    Article  Google Scholar 

  30. National Standardization of Technical Committee (2008) Standard illuminants and geometric conditions GB/T 3978-2008. China Standard Press, Beijing

    Google Scholar 

  31. Pang T, Liu J, Liu Q, Lin W (2011) Changes of photosynthetic behaviors in Kappaphycus alvarezii infected by epiphyte. eCAM 4:477–482

    Google Scholar 

  32. Pang T, Liu J, Liu Q, Zhang L, Lin W (2012) Impacts of glyphosate on photosynthetic behaviors in Kappaphycus alvarezii and Neosiphonia savatieri detected by JIP-test. J Appl Phycol 24:467–473

    CAS  Article  Google Scholar 

  33. Pang T, Liu J, Liu Q, Li H, Li JP (2015) Observations on pests and diseases affecting a eucheumatoid farm in China. J Appl Phycol 27:1975–1984

    Article  Google Scholar 

  34. Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Env Sci Pollut Res 22:4056–4075

    CAS  Article  Google Scholar 

  35. Parker HS (1974) The culture of the red algal genus Eucheuma in the Philippines. Aquaculture 3:425–439

    Article  Google Scholar 

  36. Ralph EM, Clinton JD (1976) Pigment changes and photosynthetic rates under selected wavelengths in the growing tips of Eucheuma isiforme (C. Agardh) J. Agardh var deudatum Cheney during vegetative growth. Brit Phycol J 11:165–174

    Article  Google Scholar 

  37. Shi DY, Guo SJ, Fan X (2011) A new ketosteroid from red alga Acanthophora spicifera. Chin J Oceanol Limnol 29(3):674–678

    CAS  Article  Google Scholar 

  38. Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–155

    CAS  Article  Google Scholar 

  39. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, pp 445–483

    Google Scholar 

  40. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 321–362

    Google Scholar 

  41. Vairappan CS (2006) Seasonal occurrences of epiphytic algae on the commercially cultivated red alga Kappaphycus alvarezii (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 18:611–617

    Article  Google Scholar 

  42. Vairappan CS, Chong CS, Hurtado AQ, Soya FE, Lhonner GB, Critchley A (2008) Distribution and symptoms of epiphyte infection in major carrageenophyte-producing farms. J Appl Phycol 20:477–483

    Article  Google Scholar 

  43. Vairappan CS, Chong SC, Matsunaga S (2013) Effect of epiphyte infection on physical and chemical properties of carrageenan produced by Kappaphycus alvarezii Doty (Soliericeae, Gigartinales, Rhodophyta). J Appl Phycol 26:923–931

    Article  Google Scholar 

  44. Venkataraman LV (1983) Monograph on blue-green alga Spirulina platensis—biotechnology and application. Department of Science and Technology, India 100 pp

    Google Scholar 

  45. Xu J, Gao K (2009) Growth, pigments, UV-absorbing compounds and agar yield of the economic red seaweed Gracilaria lemaneiformis (Rhodophyta) grown at different depths in the coastal waters of the South China Sea. J Appl Phycol 20:231–236

    Google Scholar 

  46. Xu N, Xiao F, Yan X, Li X, Niu R, Tseng CK (2003) Antibacterial bromophenols from the marine red alga Rhodomela confervoides. Phytochemistry 62:1221–1224

    CAS  Article  PubMed  Google Scholar 

  47. Yong WTL, Ting SH, Yong YS, Thien VY, Wong SH, Chin WL, Rodrigues KF, Anton A (2014) Optimization of culture conditions for the direct regeneration of Kappaphycus alvarezii (Rhodophyta, Solieriaceae). J Appl Phycol 26:1597–1606

    CAS  Article  Google Scholar 

  48. Zhang LT, Zhang ZS, Gao HY, Meng XL, Yang C, Liu JG, Meng QW (2012) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:23–28

    Article  Google Scholar 

  49. Zhao KF, Fan H, Zhou S, Song J (2003) Study on the salt and drought tolerance of Suaeda salsa and Kalanchoe claigremontiana under iso-osmotic salt and water stress. Plant Sci 165:837–844

    CAS  Article  Google Scholar 

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Acknowledgements

This work was financially supported by the Special Project for Marine Public Welfare Industry (grant no. 201505033) and the Marine Economy Innovation and Development Fund of Qingdao (2012). The authors would like to thank Dr. John van der Meer of the Pan-American Marine Biotechnology Association for his assistance with proofreading.

Contributions

Yongfu Li and Jianguo Liu designed the study and wrote the manuscript; Tong Pang collected the materials for the experiment; and Yongfu Li and Litao Zhang performed the experiments and analyzed the data.

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Correspondence to Jianguo Liu.

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Li, Y., Pang, T., Liu, J. et al. Light absorption and impacts of low salinities on photosynthetic behaviour in the epiphytic alga Neosiphonia savatieri (Rhodomelaceae, Rhodophyta). J Appl Phycol 29, 1673–1681 (2017). https://doi.org/10.1007/s10811-016-1046-6

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Keywords

  • Neosiphonia savatieri
  • Mean extinction coefficient
  • Eucheumatoids
  • Salinity
  • Fast chlorophyll a fluorescence