Temporal and spatial variability of mycosporine-like amino acids and pigments in three edible red seaweeds from western Ireland

  • Freddy Guihéneuf
  • Anna Gietl
  • Dagmar B. Stengel
Article

Abstract

The content of photosynthetic pigments (chlorophyll a and phycobiliproteins) and UV-absorbing mycosporine-like amino acids (MAAs) was investigated in three commercially important red macroalgae, Palmaria palmata, Chondrus crispus, and Porphyra dioica, with respect to seasonal changes at three locations in Galway Bay (western Ireland). Several parameters, including light, temperature, salinity, and nutrients, were measured over a 12-month sampling period, in an attempt to correlate changes in the content of compounds with variations in environmental factors. Pigments followed a distinct seasonal pattern, similar for the three species, which correlated in most cases with changes of seasonal environmental factors. As irradiance and temperature decreased in autumn, chlorophyll a and phycobiliprotein concentrations increased and remained high throughout winter, typically reaching maximum levels by late winter, early spring. By contrast, an increase in total MAA contents in all species was induced by increasing daily light doses and irradiance levels, from winter to spring, but without clear significant correlations with light and/or temperature. This could be explained by the low nutrient concentrations observed in summer months, limiting the synthesis and accumulation of MAAs, even when exposed to high irradiance levels. Nutrient availability, in particular nitrate, appears to be a limiting factor for the red algal species under investigation to synthetize MAA compounds when exposed to extreme light/irradiance stress. This study provides therefore the first available account of the seasonal variability of pigments and MAAs in these three commercially and ecologically important edible red seaweeds from Ireland.

Keywords

Rhodophyta Seasonal variation Light and temperature Nutrients Phycobiliproteins MAAs 

Notes

Acknowledgements

The authors acknowledge Charlotte André and Guillaume Barbarin for assistance with HPLC analysis of MAAs. The authors thank Tom Rossiter for assistance in realizing the map of sampling locations. This work was supported under the National Development Plan 2007–2013 and the Food Institutional Research Measure, administered by the Department of Agriculture, Food, and the Marine, Ireland under grant number 13/F/536.

References

  1. Aguilera J, Bischof K, Karsten U, Hanelt D (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Mar Biol 140:1087–1095CrossRefGoogle Scholar
  2. 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 39:50–58CrossRefGoogle Scholar
  3. Ammermann J (2001) Determination of orthophosphate in seawaters by flow injection analysis. QuikChem® Method 31–115–01-1-I, Methods manual, Lachat InstrumentsGoogle Scholar
  4. Athukorala Y, Trang S, Kwok C, Yuan YV (2016) Antiproliferative and antioxidant activities and mycosporine-like amino acid profiles of wild harvested and cultivated edible Canadian marine red macroalgae. Molecules 21:119CrossRefGoogle Scholar
  5. Barceló-Villalobos M, Figueroa FL, Korbee N, Álvarez-Gómez F, Abreu MH (2017) Production of mycosporine-like amino acids from Gracilaria vermiculophylla (Rhodophyta) cultured through one year in an integrated multi-trophic aquaculture (IMTA) system. Mar Biotechnol 19:246–254CrossRefPubMedGoogle Scholar
  6. Barufi JB, Korbee N, Oliveira MC, Figueroa FL (2011) Effects of N supply on the accumulation of photosynthetic pigments and photoprotectors in Gracilaria tenuistipitata (Rhodophyta) cultured under UV radiation. J Appl Phycol 23:457–466CrossRefGoogle Scholar
  7. Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Aust J Mar Freshw Res 36:785–792CrossRefGoogle Scholar
  8. Bidigare RR, van Heukelem L, Trees CC (2005) Analysis of algal pigments by high-performance-liquid-chromatography. In: Andersen (ed) Algal culturing techniques. Academic Press. London, pp 327–345Google Scholar
  9. Chopin T, Gallant T, Davison I (1995) Phosphorus and nitrogen nutrition in Chondrus crispus (Rhodophyta) - effects on total phosphorus and nitrogen-content, carrageenan production, and photosynthetic pigments and metabolism. J Phycol 31:283–293CrossRefGoogle Scholar
  10. Chopin T, Yarish C, Wilkes R, Belyea E, Lu S, Mathieson A (1999) Developing Porphyra/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J Appl Phycol 11:463–472CrossRefGoogle Scholar
  11. Cox S, Abu-Ghannam N, Gupta S (2010) An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. Int Food Res J 17:205–220Google Scholar
  12. de la Coba F, Aguilera J, Figueroa FL, de Galvez MV, Herrera E (2009) Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J Appl Phycol 21:161–169CrossRefGoogle Scholar
  13. Denis C, Morançais M, Li M, Deniaud E, Gaudin P, Wielgosz-Collin G, Barnathan G, Jaouen P, Fleurence J (2010) Study of the chemical composition of edible red macroalgae Grateloupia turuturu from Brittany (France). Food Chem 119:913–917CrossRefGoogle Scholar
  14. Ding L, Yuanyuan M, Huang B, Chen S (2013) Effects of seawater salinity and temperature on growth and pigment contents in Hypnea cervicornis J. Agardh (Gigartinales, Rhodophyta). Biomed Res Int 2013:594308PubMedPubMedCentralGoogle Scholar
  15. Eriksen NT (2008) Production of phycocyanin - a pigment with applications in biology, biotechnology, foods and medicine. Appl Microbiol Biotechnol 80:1–14CrossRefPubMedGoogle Scholar
  16. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28CrossRefGoogle Scholar
  17. Fleurence J, Levine I (eds) (2016) Seaweed in health and disease prevention. Elsevier, Amsterdam, p 476Google Scholar
  18. Figueroa FL, Escassi L, Pérez-Rodríguez E, Korbee N, Giles AD, Johnsen G (2003) 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 Photochem Photobiol B 691:21–30CrossRefGoogle Scholar
  19. Figueroa FL, Israel A, Neori A, Martínez B, Malta EJ, Put A, Inken S, Marquardt R, Abdala R, Korbee N (2010) Effect of nutrient supply on photosynthesis and pigmentation to short-term stress (UV radiation) in Gracilaria conferta (Rhodophyta). Mar Pollut Bull 60:1768–1778CrossRefPubMedGoogle Scholar
  20. Franklin LA, Kräbs G, Kuhlenkamp R (2001) Blue light and UV-A radiation control the synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae). J Phycol 37:257–270CrossRefGoogle Scholar
  21. Ganesan P, Kumar CS, Bhaskar N (2008) Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds. Bioresour Technol 99:2717–2723CrossRefPubMedGoogle Scholar
  22. Hafting JT, Craigie JS, Stengel DB, Loureiro RR, Buschmann AH, Yarish C, Edwards MD, Critchley AT (2015) Prospects and challenges for industrial production of seaweed bioactives. J Phycol 51:821–837CrossRefPubMedGoogle Scholar
  23. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  24. Huovinen P, Gómez I, Figueroa FL, Ulloa N, Morales V, Lovengreen C (2004) Ultraviolet-absorbing mycosporine-like amino acids in red macroalgae from Chile. Bot Mar 47:21–29CrossRefGoogle Scholar
  25. Hurd CL, Harrison PJ, Bischof K, Lobban CS (eds) (2014) Seaweed ecology and physiology. Cambridge University Press, CambridgeGoogle Scholar
  26. Ismail MM, Osman MEH (2016) Seasonal fluctuation of photosynthetic pigments of most common red seaweeds species collected from Abu Qir, Alexandria, Egypt. Rev Biol Mar Oceanogr 51:515–525CrossRefGoogle Scholar
  27. Kakinuma M, Coury DA, Kuno Y, Itoh S, Kozawa Y, Inagaki E, Yoshiura Y, Amano H (2006) Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Mar Biol 149:97–106CrossRefGoogle Scholar
  28. Karsten U, Sawall T, Hanelt D, Bischof K, Figueroa FL, Flores-Moya A, Wiencke C (1998a) An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions. Bot Mar 41:443–453CrossRefGoogle Scholar
  29. Karsten U, Franklin LA, Lüning K, Wiencke C (1998b) Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205:257–262CrossRefGoogle Scholar
  30. Karsten U, Wiencke C (1999) Factors controlling the formation of UV-absorbing mycosporine-like amino acids in the marine red alga Palmaria palmata from Spitsbergen (Norway). J Plant Physiol 155:407–415CrossRefGoogle Scholar
  31. Karsten U, Dummermuth A, Hoyer K, Wiencke C (2003) Interactive effects of ultraviolet radiation and salinity on the ecophysiology of two Arctic red algae from shallow waters. Polar Biol 26:249–258Google Scholar
  32. Karsten U, Escoubeyrou K, Charles F (2009) The effect of re-dissolution solvents and HPLC columns on the analysis of mycosporine-like amino acids in the eulittoral macroalgae Prasiola crispa and Porphyra umbilicalis. Helgol Mar Res 63:231–238CrossRefGoogle Scholar
  33. Kılınç B, Cirik S, Turan G, Tekogul H, Koru E (2013) Seaweeds for food and industrial applications. In: Muzzalupo I (ed) Agricultural and Biological Sciences. Food Industry, InTech, Riejeka pp 735–748Google Scholar
  34. 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 19:431–440CrossRefGoogle Scholar
  35. Kim KN, Heo SJ, Yoon WJ, Kang SM, Ahn G, Yi TH, Jeon YJ (2010) Fucoxanthin inhibits the inflammatory response by suppressing the activation of NF-κB and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur J Pharmacol 649:369–375CrossRefPubMedGoogle Scholar
  36. Korbee-Peinado NK, Díaz RTA, Figueroa FL, Helbling EW (2004) Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina. J Phycol 40:248–259CrossRefGoogle Scholar
  37. Korbee N, Figueroa FL, Aguilera J (2005a) Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photochem Photobiol B 80:71–78CrossRefPubMedGoogle Scholar
  38. Korbee N, Huovinen P, Figueroa FL, Aguilera J, Karsten U (2005b) Availability of ammonium influences photosynthesis and the accumulation of mycosporine-like amino acids in two Porphyra species (Bangiales, Rhodophyta). Mar Biol 146:645–654CrossRefGoogle Scholar
  39. Kräbs G, Bischof K, Hanelt D, Karsten U, Wiencke C (2002) Wavelength-dependent induction of UV-absorbing mycosporine-like amino acids in the red alga Chondrus crispus under natural solar radiation. J Exp Mar Biol Ecol 268:69–82CrossRefGoogle Scholar
  40. Lawrence KP, Long PF, Young AR (2017) Mycosporine-like amino acids for skin photoprotection. Curr Med Chem 24:1–16CrossRefGoogle Scholar
  41. Lee JC, Hou MF, Huang HW, Chang FR, Yeh CC, Tang JY, Chang HW (2013) Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell Int 13:55–61CrossRefPubMedPubMedCentralGoogle Scholar
  42. MacArtain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543CrossRefPubMedGoogle Scholar
  43. Marambio J, Mendez F, Ocaranza P, Rodriguez JP, Rosenfeld S, Ojeda J, Murcia S, Terrados J, Bischof K, Mansilla A (2017) Seasonal variations of the photosynthetic activity and pigment concentrations in different reproductive phases of Gigartina skottsbergii (Rhodophyta, Gigartinales) in the Magellan region, sub-Antarctic Chile. J Appl Phycol 29:721–729CrossRefGoogle Scholar
  44. Martinez B, Rico JM (2002) Seasonal variation of P content and major N pools in Palmaria palmata (Rhodophyta). J Phycol 38:1082–1089CrossRefGoogle Scholar
  45. Mouritsen OG (2017) Those tasty weeds. J Appl Phycol 29:2159–2164CrossRefGoogle Scholar
  46. Mouritsen OG, Dawczynski C, Duelund L, Jahreis G, Vetter W, Schroder M (2013) On the human consumption of the red seaweed Dulse (Palmaria palmata (L.) Weber & Mohr). J Appl Phycol 25:1777–1791CrossRefGoogle Scholar
  47. Okai Y, Hiqashi-Okai K, Yano Y, Otani S (1996) Identification of antimutagenic substances in an extract of edible red alga, Porphyra tenera (Asadusa-nori). Cancer Lett 100:235–240CrossRefPubMedGoogle Scholar
  48. Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10CrossRefPubMedGoogle Scholar
  49. Pakker H, Martins RS, Boelen P, Buma AG, Nikaido O, Breeman AM (2000) Effects of temperature on the photoreactivation of ultraviolet-b–induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341CrossRefGoogle Scholar
  50. Pangestuti R, Kim SK (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Food 3:255–266CrossRefGoogle Scholar
  51. Pereira DC, Trigueiro TG, Colepicolo P, Marinho-Soriano E (2012) Seasonal changes in the pigment composition of natural population of Gracilaria domingensis (Gracilariales, Rhodophyta). Rev Bras Farmacogn 22:874–880CrossRefGoogle Scholar
  52. Sampath-Wiley P, Neefus CD, Jahnke LS (2008) 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 361:83–91CrossRefGoogle Scholar
  53. Schmid M, Guihéneuf F, Stengel DB (2014) Fatty acid contents and profiles of 16 macroalgae collected from the Irish coast at two seasons. J Appl Phycol 26:451–463CrossRefGoogle Scholar
  54. Schmid M, Guihéneuf F, Stengel DB (2017) Ecological and commercial implications of temporal and spatial variability in the composition of pigments and fatty acids in five Irish macroalgae. Mar Biol 164:158CrossRefGoogle Scholar
  55. Schmid M, Stengel DB (2015) Intra-thallus differentiation of fatty acid and pigment profiles in some temperate Fucales and Laminariales. J Phycol 51:25–36CrossRefPubMedGoogle Scholar
  56. Sekar S, Chandramohan M (2008) Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. J Appl Phycol 20:113–136CrossRefGoogle Scholar
  57. Sinha RP, Klisch M, Gröniger A, Häder DP (2000) Mycosporine-like amino acids in the marine red alga Gracilaria cornea - effects of UV and heat. Environ Exp Bot 43:33–43CrossRefGoogle Scholar
  58. Smith AM, Cave RR (2012) Influence of fresh water, nutrients and DOC in two submarine-groundwater-fed estuaries on the west of Ireland. Sci Total Environ 438:260–270CrossRefPubMedGoogle Scholar
  59. Smith P, Bogren K (2001) Determination of nitrate and/or nitrite in brackish or seawater by flow injection analysis colorimeter. QuikChem® Method 31–107–04-1-E, Methods manual, Lachat InstrumentsGoogle Scholar
  60. Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29:483–501CrossRefPubMedGoogle Scholar
  61. Stengel DB, Connan S (eds) (2015) Natural products from marine algae: methods and protocols. Springer protocols, Methods in Molecular Biology 1308. Humana Press, Springer, New York, p 439Google Scholar
  62. Stengel DB, Dring MJ (1998) Seasonal variation in the pigment content and photosynthesis of different thallus regions of Ascophyllum nodosum (Fucales, Phaeophyta) in relation to position in the canopy. Phycologia 37:259–268CrossRefGoogle Scholar
  63. Suh SS, Hwang H, Park M, Seo H, Kim HS, Lee J, Moh S, Lee TK (2014) Anti-inflammation activities of mycosporine-like amino acids (MAAs) in response to UV radiation suggest potential anti-skin aging activity. Mar Drugs 12:5174–5187CrossRefPubMedPubMedCentralGoogle Scholar
  64. Talarico L, Maranzana G (2000) Light and adaptive responses in red macroalgae: an overview. J Photochem Photobiol B 56:1–11CrossRefPubMedGoogle Scholar
  65. Talarico LB, Zibetti RGM, Faria PCS, Scolaro LA, Duarte MER, Noseda MD, Pujol CA, Damonte EB (2004) Anti-herpes simplex virus activity of sulfated galactans from the red seaweed Gymnogongrus griffithsiae and Cryptonemia crenulata. Int J Biol Macromol 34:63–71CrossRefPubMedGoogle Scholar
  66. Tartarotti B, Sommaruga R (2002) The effect of different methanol concentrations and temperatures on the extraction of mycosporine-like amino acids (MAAs) in algae and zooplankton. Arch Hydrobiol 154:691–703CrossRefGoogle Scholar
  67. Torres A, Enk CD, Hochberg M, Srebnik M (2006) Porphyra-334, a potential natural source for UVA protective sunscreens. Photochem Photobiol Sci 5:432–435CrossRefPubMedGoogle Scholar
  68. Vincent WF, Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment, Cambridge environmental chemistry series, vol 10. Cambridge University Press, New York, pp 149–176CrossRefGoogle Scholar
  69. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjørnland T, Repeta D, Welschmeyer N (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77:183–196CrossRefGoogle Scholar
  70. Yabuta Y, Fujimura H, Kwak CS, Enomoto T, Watanabe F (2010) Antioxidant activity of the phycoerythrobilin compound formed from a dried Korean purple laver (Porphyra sp.) during in vitro digestion. Food Sci Technol Res 16:347–352CrossRefGoogle Scholar
  71. Zacharias M (2012) Ecophysiological studies of selected macro- and microalgae: production of organic compounds and climate change interactions. Unpublished PhD thesis. National University of Ireland Galway, IrelandGoogle Scholar

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Authors and Affiliations

  1. 1.Botany and Plant Science, School of Natural Sciences, Ryan Institute for Environmental, Marine and Energy ResearchNational University of Ireland GalwayGalwayIreland

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