Photosynthetica, 2018 (vol. 56), issue 4

Photosynthetica 2018, 56(4):1093-1106 | DOI: 10.1007/s11099-018-0805-9

Physiological responses of Pterocladiella capillacea (Rhodophyta, Gelidiales) under two light intensities

T.B. Harb1,*, A. Nardelli1, F. Chow1
1 Institute of Bioscience, University of São Paulo, São Paulo, SP, Brazil

Macroalgae must be able to survive in conditions of different light intensities with no damage to their physiological performance or vital processes. Irradiance can stimulate the biosynthesis of certain photoprotective compounds of biotechnological interest, such as pigments and proteins. Pterocladiella capillacea is a shade-grown alga, which play a role key in the balance of marine ecosystems. In addition, it is considered one of the best sources of bacteriological agar and agarose with a wide pharmacological potential. In order to evaluate the photosensitivity in P. capillacea under 60 (control) and moderate light intensity of 300 μmol(photon) m-2 s-1, photosynthetic performance and chemical composition were assessed. P. capillacea showed photosensitivity without evidence of photodamage. The results indicate the possibility to increase a growth rate and probably infer productivity in long-term cultivation by stimulation at moderate light intensity. Increasing photosynthetic pigment and protein contents were also observed under medium light, an interesting result for functional ingredient approaches.

Keywords: algae; chlorophyll fluorescence; growth rate; pigments; productivity; radiation

Received: February 21, 2017; Accepted: August 18, 2017; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

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Harb, T.B., Nardelli, A., & Chow, F. (2018). Physiological responses of Pterocladiella capillacea (Rhodophyta, Gelidiales) under two light intensities. Photosynthetica, 56(4), 1093-1106. doi: 10.1007/s11099-018-0805-9.
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    References

    1. Adir N., Zer H., Shochat S. et al.: Photoinhibition: a historical perspective.-Photosynth. Res. 76: 343-370, 2003. Go to original source...
    2. Andria J.R., Vergara J.J., Perez-Llorens J.L.: Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cádiz, Spain, cultured under different inorganic carbon and nitrogen levels.-Eur. J. Phycol. 34: 497-504, 1999. Go to original source...
    3. Asada K.: Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress.-In: Baker N.R., Bowyer J.R. (ed.): Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Pp. 129-142. Bios. Sci. Publ., Oxford 1994.
    4. Balboa E.M., Conde E., Moure A., et al.: In vitro antioxidant properties of crude extracts and compounds from brown algae.-Food Chem. 138: 1764-1785, 2013. Go to original source...
    5. Bautista A.I.N., Necchi O. Jr.: Photoacclimation in a tropical population of Cladophora glomerata (L.) Kützing 1843 (Chlorophyta) from southeastern.-Braz. J. Biol. 68: 129-36, 2008.
    6. Beach K.S., Smith C.M., Okano R.: Experimental analysis of rhodophyte photoacclimation to PAR and UV-radiation using in vivo absorbance spectroscopy.-Bot. Mar. 43: 525-536, 2000.
    7. Betancor S., Tuya F., Gil-Díaz T. et al.: Effects of a submarine eruption on the performance of two brown seaweeds.-J. Sea Res. 87: 68-78, 2014. Go to original source...
    8. Bradford M.: A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248-254, 1976. Go to original source...
    9. Carnicas E., Jiménez C., Niell F.X.: Effects of changes of irradiance on the pigment composition of Gracilaria tenuistipitata var. liui Zhang et Xia.-J. Photoch. Photobio. B 50: 149-158, 1999. Go to original source...
    10. Chaloub R.M, Reinert F., Nassar C.A.G. et al.: Photosynthetic properties of three Brazilian seaweeds.-Rev. Bras. Bot. 33: 371-374, 2010. Go to original source...
    11. Cherry J.H., Nielsen B.L.: Metabolic engineering of chloroplasts for abiotic stress tolerance.-In: Daniell H., Chase C.D. (ed.): Molecular Biology and Biotechnology of Plant Organelles. Pp. 513-525. Springer, Dordrecht 2004. Go to original source...
    12. Collén P.N., Camitz A., Hancock R.D. et al.: Effect of nutrient deprivation and resupply on metabolites and enzymes related to carbon allocation in Gracilaria tenuistipitata (Rhodophyta).-J. Phycol. 40: 305-314, 2004. Go to original source...
    13. Copertino M.S., Cheshire A., Watling J.: Photoinhibition and photoacclimation of turf algal communities on a temperate reef, after in situ transplantation experiments.-J. Phycol. 42: 580-592, 2006. Go to original source...
    14. Coutinho R., Yoneshigue Y.: Diurnal variation in photosynthesis vs. irradiance curves from "sun" and "shade" plants of Pterocladia capillacea (Gmelin) Bornet et Thuret (Gelidiaciaceae: Rhodophyta) from Cabo Frio, Rio De Janeiro, Brazil.-J. Exp. Mar. Biol. Ecol. 118: 217-228, 1988. Go to original source...
    15. Del Campo J.A., García-Gonzáles M., Guerrero M.G.: Outdoor cultivation of microalgae for carotenoid production: current states and perspectives.-Appl. Microbiol. Biotechnol. 74: 1763-1774, 2007. Go to original source...
    16. Donkor V.A., Häder D.P.: Effects of ultraviolet irradiation on photosynthetic pigments in some filamentous cyanobacteria.-Aquat. Microb. Ecol. 11: 143-149, 1996. Go to original source...
    17. dos Santos R.W., Schmidt É.C., Martins R.P. et al.: Effects of cadmium on growth, photosynthetic pigments, photosynthetic performance, biochemical parameters and structure of chloroplasts in the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales).-Am. J. Plant Sci. 3: 1077-1084, 2012.
    18. Edwards P.: Illustrated guide to the seaweeds and sea grasses in the vicinity of Porto Aransas, Texas.-In: Edwards P. (ed.): Seaweeds and Sea Grasses: Contributions in Marine Science, vol. 15. Pp. 132. B. J. Copeland, Texas 1970.
    19. Falkowski P.G.: Light-shade adaptation in marine phytoplankton.-In: Falkowski P.G. (ed.): Primary Production in the Sea. Pp. 531. Plenum Press, New York 1980. Go to original source...
    20. Figueroa F.L., Conde-Álvarez R., Gómez I.: Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions.-Photosynth. Res. 75: 259-275, 2003a. Go to original source...
    21. Figueroa F.L., Escassi L., Perez-Rodríguez E. et al.: Effects of short-term irradiation on photoinhibition and accumulation of mycosporine-like amino acids in sun and shade species of the red algal genus Porphyra.-J. Photoch. Photobio. B. 69: 21-30, 2003b. Go to original source...
    22. Figueroa F.L., Martínez B., Israel A. et al.: Acclimation of red sea macroalgae to solar radiation: photosynthesis and thallus absorptance.-Aquat. Biol. 7: 159-172, 2009. Go to original source...
    23. Figueroa F.L., Domínguez-González B., Korbee N.: Vulnerability and acclimation to increased UVB radiation in three intertidal macroalgae of different morpho-functional groups.-Mar. Environ. Res. 97: 30-38, 2014a.
    24. Figueroa F.L, Barufi B.J., Malta E.J. et al.: Short-term effects of increased CO2, nitrate and temperature on three Mediterranean macroalgae: photosynthesis and biochemical composition.-Aquat. Biol. 22: 177-193, 2014b. Go to original source...
    25. Franklin L.A., Larkum A.W.D.: Multiple strategies for a high light existence in a tropical marine macroalga.-Photosynth. Res. 53: 149-159, 1997. Go to original source...
    26. ranklin L.A., Osmond C.B., Larkym A.W.D.: Photoinhibition, UV-B and Algal Photosynthesis. Pp. 352-375. Kluwer Academic Publishers, Berlin 2003. Go to original source...
    27. Gal-Or S., Israel A.: Growth responses of Pterocladiella capillacea (Rhodophyta) in laboratory and outdoor cultivation.-J. Appl. Phycol. 16: 195-202, 2004. Go to original source...
    28. Gantt E.: Pigmentation and photoacclimation.-In: Cole K.M., Sheath R.G. (ed.): Biology of the Red Algae. Pp. 203-219. Cambridge University Press, Cambridge 1990.
    29. Gómez I., Huovinen P.: Morpho-functional patterns and zonation of South Chilean seaweeds: the importance of photosynthetic and bio-optical traits.-Mar. Ecol. Prog. Ser. 422: 77-91, 2011. Go to original source...
    30. Gómez I., López-Figueroa F., Ulloa N. et al.: Patterns of photosynthesis in 18 species of intertidal macroalgae from southern Chile.-Mar. Ecol. Prog. Ser. 270: 103-116, 2004. Go to original source...
    31. Gordillo F.J.L, Jiménez C., Goutx M. et al.: Effects of CO2 and nitrogen supply on the biochemical composition of Ulva rigida with especial emphasis on lipid class analysis.-J. Plant Physiol. 158: 367-373, 2001. Go to original source...
    32. Goss R., Jacob T.: Regulation and function of xanthophyll cycledependent photoprotection in algae.-Photosynth. Res. 106: 103-122, 2010. Go to original source...
    33. Grobbelaar J.U., Kurano N.: Use of photoacclimation in the design of a novel photobioreactor to achieve high yields in algal mass cultivation.-J. Appl. Phycol. 15: 121-126, 2003. Go to original source...
    34. Grzymski J., Johnsen G., Sakshaug E.: The significance of intracellular self-shading on the bio-optical properties of brown, red and green macroalgae.-J. Appl. Phycol. 33: 408-414, 1997. Go to original source...
    35. Guimarães S.M.P.B.: A revised checklist of benthic marine Rhodophyta from the state of Espírito Santo, Brazil.-Bol. Inst. Bot. 17: 143-194, 2006.
    36. Hanelt D., Figueroa F.L.: Physiological and photomorphogenic effects of light on marine macrophytes.-In: Wiencke C., Bischof K. (ed.): Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization, Vol. 219. Pp. 3-23. Springer, Heidelberg 2012. Go to original source...
    37. Hanelt D., Hawes I., Rae R.: Reduction of UV-B radiation causes an enhancement of photoinhibition in high light stressed aquatic plants from New Zealand lakes.-J. Photoch. Photobio. B 84: 89-102, 2006. Go to original source...
    38. He L.H., Wu M., Qian P.Y. et al.: Effects of co-culture and salinity on the growth and agar yield of Gracilaria tenuistipitata var. liui Zhang et Xia.-Chin. J. Oceanol. Limnol. 20: 365-370, 2002.
    39. Heldt H-W., Piechulla B.: Plant Biochemistry, 4th ed. Pp. 618. Elsevier, Burlington 2011.
    40. Hideg E., Spetea C., Vass I.: Singlet oxygen and free-radical production during acceptor-induced and donor-side-induced photoinhibition: studies with spin-trapping EPR spectroscopy.-BBA-Bioenergenetics 1186: 143-152, 1994. Go to original source...
    41. Hou X., Hou H.J.: Roles of manganese in photosystem II dynamics to irradiations and temperatures.-Front Biol. 8: 312-322, 2013. Go to original source...
    42. Huertas E., Montero O., Lubián L.M.: Effects of dissolved inorganic carbon availability on growth, nutrient uptake and chlorophyll fluorescence of two species of marine microalgae.-Aquacult. Eng. 22: 181-197, 2000. Go to original source...
    43. Jassby A.D., Platt T.: Mathematical formulation of the relationship between photosynthesis and light for phytoplankton.-Limnol. Oceanogr. 21: 540-547, 1976. Go to original source...
    44. Klughammer C., Schreiber U.: Complementary PSII quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method.-PAM Appl. Notes. 1: 27-35, 2008.
    45. Kursar T.A., van der Meer J., Alberte R.S.: Light-harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analyses of pigments mutation.-Plant Physiol. 73: 353-360, 1983. Go to original source...
    46. Lee T.M., Shiu C.T.: Implications of mycosporine-like amino acid and antioxidant defences in UV-B radiation tolerance for the algae species Pterocladiella capillacea and Gelidium amansii.-Mar. Environ. Res. 67: 8-16, 2009.
    47. Levy I., Gantt E.: Light acclimation in Porphyridium purpureum (Rhodophyta): growth, photosynthesis, and phycobilisomes.-J. Appl. Phycol. 24: 452-458, 1988.
    48. Lichtenthaler H.K., Buschmann C.: Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy.-In: Wrolstad R.E., Acree T.E., An H. et al. (ed.): Current Protocols in Food Analytical Chemistry. Pp. F4.3.1-F4.3.8. John Wiley & Sons, New York 2001. Go to original source...
    49. Liu F., Pang S.J.: Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmate.-J. Exp. Mar. Biol. Ecol. 382: 82-87, 2010. Go to original source...
    50. MacIntyre H.L., Kana T.M., Geider R.J.: The effect of water motion on short-term rates of photosynthesis by marine phytoplankton.-Trends Plant Sci. 5: 12-17, 2000. Go to original source...
    51. Martínez B., Rico J.: Changes in nutrient content of Palmaria palmata in response to changes in nutrient to variable light and upwelling in northern Spain.-J. Phycol. 44: 50-59, 2008. Go to original source...
    52. Martins A.P., Chow F., Yokoya N.S.: [In vitro assay of nitrate reductase enzyme and effect of nitrate and phosphate availability in colour strains of Hypnea musciformis (Wulfen) J. V. Lamour. E. (Gigartinales, Rhodophyta)].-Rev. Bras. Bot. 32: 635-645, 2009. [In Portuguese] Go to original source...
    53. Martone P. T., Alyono M., Stites S.: Bleaching of an intertidal coralline alga: untangling the effects of light, temperature and desiccation.-Mar. Ecol. Prog. Ser. 416: 57-67, 2010. Go to original source...
    54. Maxwell K., Johnson G.N.: Chlorophyll fluorescence: a practical guide.-J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    55. Mercado J.M., Jiménez C., Niell F.X. et al.: Comparison of methods for measuring light absorption by algae and their application to the estimation of package effect.-Sci. Mar. 60: 39-45, 1996.
    56. Nascimento E.F.I., Rosso S.: [Fauna associated with benthic marine macroalgae (Rhodophyta and Phaeophyta) from São Sebastião, São Paulo].-Rev. Bras. Ecol. 11: 38-52, 2007. [In Portuguese]
    57. Necchi O. Jr.: Light-related photosynthetic characteristic of freshwater Rhodophyta.-Aquat. Bot. 82: 193-20, 2005. Go to original source...
    58. Nishihara G.N., Terada R., Noro T.: Effect of temperature and irradiance on the uptake of ammonium and nitrate by Laurencia brongniartii (Rhodophyta, Ceramiales).-J. Appl. Phycol. 17: 371-377, 2005. Go to original source...
    59. Nishiyama Y., Allakhverdiev S., Yamamoto H. et al.: Singlet oxygen inhibits the repair of photosystem II by suppressing translation elongation of the D1 protein in Synechocystis sp.-Biochemistry 43: 11321-11330, 2004. Go to original source...
    60. Nyvall-Cóllen P., Camitz A., Hancock R.D. et al.: Effect of nutrient deprivation and resupply on metabolites and enzymes related to carbon allocation in Gracilaria tenuistipitata (Rhodophyta).-J. Appl. Phycol. 40: 305-314, 2004.
    61. Oliveira E.C., Saito R.M., Neto J.F.S. et al.: Temporal and spatial variation in agar from a population of Pterocladia capillacea (Gelidiales, Rhodophyta) from Brazil.-Hydrobiologia 326: 501-504, 1996. Go to original source...
    62. Park J.J., Han T., Choi E.M.: Differences in the oxidative stress and antioxidant responses of three marine macroalgal species upon UV exposure.-Toxicol. Environ. Health Sci. 8: 101-107, 2016. Go to original source...
    63. Penniman C.A., Mathieson A.C., Penniman C.E.: Reproductive phenology and growth of Gracilaria tikvahiae McLachlan (Gigartinales, Rhodophyta) in the Great Bay Estuary, New Hampshire.-Bot. Mar. 29: 147-154, 1986. Go to original source...
    64. Polo L.K., Felix M.R.L., Kreusch M. et al.: Metabolic profile of the brown macroalga Sargassum cymosum (Phaeophyceae, Fucales) under laboratory UV radiation and salinity conditions.-J. Appl. Phycol. 90: 560-571, 2014.
    65. Ramus J., Rosenberg G.: Diurnal photosynthetic performance of seaweeds measured under natural conditions.-Mar. Biol. 56: 21-28, 1980. Go to original source...
    66. Rohácek K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.-Photosynth. Res. 40: 13-29, 2002. Go to original source...
    67. Sampath-Wiley P., Neefus C., Jahnke L.: Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales).-J. Exp. Mar. Biol. Ecol. 361: 83-91, 2008. Go to original source...
    68. Schmidt E.C., Pereira B., Pontes C.L.: Alterations in architecture and metabolism induced by ultraviolet radiation-B in the carragenophyte Chondracanthus teedei Rhodophyta, Gigartinales.-Protoplasma 249: 353-367, 2012. Go to original source...
    69. Schreiber U., Schliwa U., Bilger W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.-Photosynth. Res. 10: 51-62, 1986. Go to original source...
    70. Schreiber U., Neubauer C.: O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence.-Photosynth. Res. 25: 279-293, 1990. Go to original source...
    71. Schubert N., García-Mendoza E.: Photoinhibition in red algal species with different carotenoid profiles.-J. Phycol. 44: 1437-1446, 2008. Go to original source...
    72. Schubert N., García-Mendoza E., Enríquez S.: Is the photoacclimation response of Rhodophyta conditioned by the species carotenoid profile?-Limnol. Oceanogr. 56: 2347-2361, 2011.
    73. Serra D.R.: [Gracilariopsis tenuifrons (Gracilariales-Rhodophyta) Response to Irradiance Stimuli in vitro].-Masters Dissertation. Pp. 97. Institute of Bioscience, University of São Paulo, São Paulo 2013. [In Portuguese]
    74. Sudatti D.B., Fujii M.T., Rodrigues S.V.: Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta).-Mar. Biol. 158: 1439-1446, 2011. Go to original source...
    75. Smit A.J.: Nitrogen uptake by Gracilaria gracilis (Rhodophyta): adaptations to a temporally variable nitrogen environment.-Bot. Mar. 45: 196-209, 2002. Go to original source...
    76. Takahashi S., Badger M.R.: Photoprotection in plants: a new light on photosystem II damage.-Trends Plant Sci. 16: 53-60, 2011. Go to original source...
    77. Takahashi S., Murata N.: How do environmental stress accelerate photoinhibition?-Trends Plant Sci. 3: 178-182, 2008. Go to original source...
    78. Tala F., Chow F.: Phenology and photosynthetic performance of Porphyra spp. (Bangiophyceae, Rhodophyta): seasonal and latitudinal variation in Chile.-Aquat. Bot. 113: 107-116, 2014. Go to original source...
    79. Torres P.B., Chow F., Santos D.Y.A.C.: Growth and photosynthetic pigments of Gracilariopsis tenuifrons (Rhodophyta, Gracilariaceae) under high light in vitro culture.-J. Appl. Phycol. 27: 1243-1251, 2014.
    80. Ursi S., Plastino E.M.: [Growth of reddish and light green strains of Gracilaria sp. (Gracilariales, Rhodophyta) in two culture media: analysis of different reproductive phases].-Rev. Bras. Bot. 24: 587-594, 2001. [In Portuguese]
    81. Ursi S., Pedersén M., Plastino E. et al.: Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta).-Mar. Biol. 142: 997-1007, 2003. Go to original source...
    82. Wanderley A.: [Effect of Nitrate Availability on Growth, Nitrate Reductase Activity, Chemical Composition and Nitrate and Phosphate Uptake in Gracilariopsis tenuifrons (Gracilariales, Rhodophyta)].-Masters Dissertation. Pp. 140. Institute of Bioscience, University of São Paulo, São Paulo, 2009. [In Portuguese]
    83. Yakovleva I.M., Titlyanov E.A.: Effect of high visible and UV irradiance on subtidal Chondrus crispus: stress photoinhibition and protective mechanisms.-Aquat. Bot. 71: 47-61, 2001. Go to original source...
    84. Zubia M., Freile-Pelegrín Y., Robledo D.: Photosynthesis, pigment composition and antioxidant defences in the red alga Gracilariopsis tenuifrons (Gracilariales, Rhodophyta) under environmental stress.-J. Phycol. 26: 2001-2010, 2014.

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