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

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Abstract

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.

Additional key words

algae chlorophyll fluorescence growth rate pigments productivity radiation 

Abbreviations

A

absorptance

Ab

absorbance

APC

allophycocyanin

DM

dry mass

Car

carotenoids

Chl

chlorophyll

CL

control irradiance of 60 μmol(photon) m–2 s–1

ETR

electron transport rate

ETRMAX

maximal electron transport rate

FM

fresh mass

FV/FM

maximal quantum yield of PSII photochemistry

GR

growth rate

IK

saturation irradiance

ML

irradiance of 300 μmol(photon) m–2 s–1

PC

phycocyanin

PE

phycoerythrin

PMAX

maximum photosynthesis

TSP

total soluble proteins

UV

ultraviolet

VSES

von Stosch enrichment solution

ΦPSII

effective quantum yield of PSII photochemistry

Y(PSII)

photochemical quenching

Y(NO)

nonregulated nonphotochemical quenching

Y(NPQ)

regulated nonphotochemical quenching

α

photosynthetic efficiency.

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References

  1. Adir N., Zer H., Shochat S. et al.: Photoinhibition: a historical perspective.–Photosynth. Res. 76: 343–370, 2003.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  26. Franklin L.A., Osmond C.B., Larkym A.W.D.: Photoinhibition, UV-B and Algal Photosynthesis. Pp. 352–375. Kluwer Academic Publishers, Berlin 2003.Google Scholar
  27. Gal-Or S., Israel A.: Growth responses of Pterocladiella capillacea (Rhodophyta) in laboratory and outdoor cultivation.–J. Appl. Phycol. 16: 195–202, 2004.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  32. Goss R., Jacob T.: Regulation and function of xanthophyll cycledependent photoprotection in algae.–Photosynth. Res. 106: 103–122, 2010.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  39. Heldt H-W., Piechulla B.: Plant Biochemistry, 4th ed. Pp. 618. Elsevier, Burlington 2011.Google Scholar
  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.CrossRefGoogle Scholar
  41. Hou X., Hou H.J.: Roles of manganese in photosystem II dynamics to irradiations and temperatures.–Front Biol. 8: 312–322, 2013.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  43. Jassby A.D., Platt T.: Mathematical formulation of the relationship between photosynthesis and light for phytoplankton.–Limnol. Oceanogr. 21: 540–547, 1976.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  47. Levy I., Gantt E.: Light acclimation in Porphyridium purpureum (Rhodophyta): growth, photosynthesis, and phycobilisomes.–J. Appl. Phycol. 24: 452–458, 1988.Google Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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]CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  54. Maxwell K., Johnson G.N.: Chlorophyll fluorescence: a practical guide.–J. Exp. Bot. 51: 659–668, 2000.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  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]Google Scholar
  57. Necchi O. Jr.: Light-related photosynthetic characteristic of freshwater Rhodophyta.–Aquat. Bot. 82: 193-20, 2005.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  65. Ramus J., Rosenberg G.: Diurnal photosynthetic performance of seaweeds measured under natural conditions.–Mar. Biol. 56: 21–28, 1980.CrossRefGoogle Scholar
  66. Roháček K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.–Photosynth. Res. 40: 13–29, 2002.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  70. Schreiber U., Neubauer C.: O2-dependent electron flow, membrane energization and the mechanism of non-photo chemical quenching of chlorophyll fluorescence.–Photosynth. Res. 25: 279–293, 1990.CrossRefPubMedGoogle Scholar
  71. Schubert N., García-Mendoza E.: Photoinhibition in red algal species with different carotenoid profiles.–J. Phycol. 44: 1437–1446, 2008.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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]Google Scholar
  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.CrossRefGoogle Scholar
  75. Smit A.J.: Nitrogen uptake by Gracilaria gracilis (Rhodophyta): adaptations to a temporally variable nitrogen environment.–Bot. Mar. 45: 196–209, 2002.CrossRefGoogle Scholar
  76. Takahashi S., Badger M.R.: Photoprotection in plants: a new light on photosystem II damage.–Trends Plant Sci. 16: 53–60, 2011.CrossRefPubMedGoogle Scholar
  77. Takahashi S., Murata N.: How do environmental stress accelerate photoinhibition?–Trends Plant Sci. 3: 178–182, 2008.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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]CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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]Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar

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© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Institute of BioscienceUniversity of São PauloSão Paulo, SP, CEPBrazil

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