Biofiltration of fishpond effluents and accumulation of N-compounds (phycobiliproteins and mycosporine-like amino acids) versus C-compounds (polysaccharides) in Hydropuntia cornea (Rhodophyta)

Marine Pollution Bulletin

Volumn 64, Issue 2, 2012, Pages 310-318

  Figueroa, Félix L ^a   Korbee, Nathalie ^a   Abdala, Roberto ^a   Jerez, Celia G ^a   López de la Torre, Mayra ^b   Güenaga, Leire ^c   Larrubia, María A ^a   Gómez Pinchetti, Juan L ^c  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b CENTRO DE INVESTIGACIÓN CIENTÍFICA Y DE EDUCACIÓN SUPERIOR DE ENSENADA   (Mexico)

^c UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

Author keywords

Biliprotein; Biofiltration; Fishpond effluent; Hydropuntia cornea; Mycosporine like amino acid; Polysaccharide

Indexed keywords

BILIPROTEIN; HYDROPUNTIA CORNEA; IMMUNOSTIMULANTS; MYCOSPORINE-LIKE AMINO ACIDS; N-COMPOUNDS; PHOTOINHIBITION; PHYCOBILIPROTEINS; POSITIVE EFFECTS; RHODOPHYTA;

ALGAE; AMINO ACIDS; BIOFILTERS; POLYSACCHARIDES; QUANTUM YIELD;

BIOFILTRATION;

AMINO ACID; CARBON; CHLOROPHYLL; MYCOSPORINE LIKE AMINO ACID; NITROGEN; PHYCOBILIPROTEIN; POLYSACCHARIDE; SEA WATER; UNCLASSIFIED DRUG;

AMINO ACID; BIOACCUMULATION; BIOFILTRATION; BIOMASS; EFFLUENT; INHIBITION; MARINE POLLUTION; ORGANIC NITROGEN COMPOUND; POLYSACCHARIDE; PROTEIN; RED ALGA;

ARTICLE; BIOACCUMULATION; BIOFILTRATION; BIOMASS; CONTROLLED STUDY; EFFLUENT; GREENHOUSE; NONHUMAN; PHOTOINHIBITION; PHOTOSYNTHESIS; PHOTOSYSTEM II; POND EFFLUENT; QUANTUM YIELD; RED ALGA; SOLAR RADIATION; ULTRAVIOLET RADIATION;

AMINO ACIDS; BIOMASS; FILTRATION; LIGHT; NITROGEN COMPOUNDS; PHOTOSYNTHESIS; POLYSACCHARIDES; RHODOPHYTA; WASTE DISPOSAL, FLUID;

ALGAE; HYDROPUNTIA CORNEA; RHODOPHYTA;

EID: 84856245876     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2011.11.012     Document Type: Article

References (69)

1. Abdala-Díaz R.T., Chabrillón M., Cabello-Pasini A., Gómez-Pinchetti J., Figueroa F.L. Characterization of polysaccharides from Hypnea spinella (Gigartinales) and Halopithys incurva (Ceramiales) and their effect on RAW 264.7 macrophage activity. J. Appl. Phycol. 2011, 23:523-528.
2. Abreu, M.H., Pereira, R., Korbee, N., Figueroa, F.L., Buschmann, A.H., Yarish, C., Sousa-Pinto, I., 2010. Sustainable exploration of a non-indigenous species: the case study of Gracilaria vermiculophylla (Ohmi) Papenfuss in Portugal. XXth International Seaweed Symposium book of abstract, pp. 43. Ensenada, Mexico.
3. Abreu M.H., Pereira R., Yarish C., Buschmann A.H., Sousa-Pinto I. IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 2011, 312:77-87.
4. Aguirre-von-Wobeser E., Figueroa F.L., Cabello-Pasini A. Effect of UV radiation on photoinhibition of marine macrophytes in culture systems. J. Appl. Phycol. 2000, 12:159-168.
5. Altamirano M., Flores-Moya A., Figueroa F.L. Long-term effects of natural sunlight under various ultraviolet radiation conditions on growth and photosynthesis of intertidal Ulva rigida (Chlorophyceae) cultivated in situ. Bot. Mar. 2000, 43:119-126.
6. Bandaranayake W.M. Mycosporines: are they nature's sunscreens?. Nat. Prod. Rep. 1998, 15:159-172.
7. Beer S., Eshel A. Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Aust. J. Mar. Fresh. Res. 1985, 36:785-792.
8. Bolton, J., Robertson-Andersson, D.M., Troell, M., Halling, C., 2006. Integrated system incorporates seaweeds in South African abalone culture. Global Aquaculture Advocate, vol. 9, pp. 54-55.
9. Boussiba S., Richmond A.E. C-phycocyanin as a storage protein in the blue-green-alga Spirulina platensis. Arch. Microbiol. 1980, 125:143-147.
10. Cabello-Pasini A., Aguirre-von-Wobeser E., Figueroa F.L. Photoinhibition of photosynthesis in Macrocystis pyrifera (Phaeophyceae), Chondrus crispus (Rhodophyceae) and Ulva lactuca (Chlorophyceae) in outdoor culture systems. J. Photoch. Photobio. B 2000, 57:169-178.
11. Castro R., Piazzon M.C., Zarra I., Leiro J., Noya M., Lamas J. Stimulation of turbot phagocytes by Ulva rigida C. Agardh polysaccharides. Aquaculture 2006, 254:9-20.
12. Castro R., Zarra I., Lamas J. Water-soluble seaweed extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture 2004, 229:67-78.
13. Cohen I., Neori A. Ulva lactuca biofilters for marine fishpond effluents I. Ammonia uptake kinetics and nitrogen-content. Bot. Mar. 1991, 34:475-482.
14. Conde F.R., Churio M.S., Previtali C.M. The photoprotector mechanism of mycosporine-like amino acids. Excited-state properties and photostability of porphyra-334 in aqueous solution. J. Photoch. Photobio. B 2000, 56:139-144.
15. Dang H.T., Lee H.J., Yoo E.S., Shinde P.B., Lee Y.M., Hong J., Kim D.K., Jung J.H. Anti-inflammatory constituents of the red alga Gracilaria verrucosa and their synthetic analogues. J. Nat. Prod. 2008, 71:232-240.
16. de la Coba F., Aguilera J., Figueroa F.L., de Gálvez M.V., Herrera E. Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J. Appl. Phycol. 2009, 21:161-169.
17. Deboer J., Ryther J. Potential yields from a waste-recycling algal mariculture system. The Marine Plant Biomass of the Pacific Northwest Coast 1977, 231-248. Oregon State University Press, Oregon. K. RW (Ed.).
18. Díaz-Rosales P., Chabrillon M., Abdala R.T., Figueroa F.L., Balebona M.C., Moriñigo M.A. Effect of dietary administration of Porphyridium cruentum on the respiratory burst activity of sole, Solea senegalensis (Kaup), phagocytes. J. Fish. Dis. 2008, 31:489-495.
19. Díaz-Rosales P., Felices C., Abdala R., Figueroa F.L., Pinchetti J.L.G., Moriñigo M.A., Balebona M.C. In vitro effect of the red alga Hydropuntia cornea (J. Agardh) on the respiratory burst activity of sole (Solea senegalensis, Kaup 1858) phagocytes. Aquac. Res. 2007, 38:1411-1418.
20. Duarte C.M. Nutrient concentration of aquatic plants - patterns across species. Limnol. Oceanogr. 1992, 37:882-889.
21. Dunlap W.C., Yamamoto Y. Small-molecule antioxidants in marine organisms - antioxidant activity of mycosporine-glycine. Comp. Biochem. Phys. B 1995, 112:105-114.
22. Fábregas J., García D., Fernández-Alonso M., Rocha A.I., Gómez-Puertas P., Escribano J.M., Otero A., Coll J.M. In vitro inhibition of the replication of haemorrhagic septicaemia virus (VHSV) and African swine fever virus (ASFV) by extracts from marine microalgae. Antivir. Res. 1999, 44:67-73.
23. Figueroa F.L., Aguilera J., Jiménez C., Vergara J.J., Robles M.D., Niell F.X. Growth, pigment synthesis and nitrogen assimilation in the red alga Porphyra sp (Bangiales, Rhodophyta) under blue and red light. Sci. Mar. 1995, 59:9-20.
24. Figueroa F.L., Bueno A., Korbee N., Santos R., Mata L., Schuenhoff A. Accumulation of mycosporine-like amino acids in Asparagopsis armata grown in tanks with fishpond effluents of gilthead sea bream, Sparus aurata. J. World Aquacult. Soc. 2008, 39:692-699.
25. Figueroa F.L., Israel A., Neori A., Martinez B., Malta E.J., Ang P., Inken S., Marquardt R., Korbee N. Effects of nutrient supply on photosynthesis and pigmentation in Ulva lactuca (Chlorophyta): responses to short-term stress. Aquat. Biol. 2009, 7:173-183.
26. Figueroa F.L., Israel A., Neori A., Martinez B., Malta E.J., Put A., Inken S., Marquardt R., Abdala R., Korbee N. Effect of nutrient supply on photosynthesis and pigmentation to short-term stress (UV radiation) in Gracilaria conferta (Rhodophyta). Mar. Pollut. Bull. 2010, 60:1768-1778.
27. Figueroa F.L., Santos R., Conde-Alvarez R., Mata L., Pinchetti J.L.G., Matos J., Huovinen P., Schuenhoff A., Silva J. The use of chlorophyll fluorescence for monitoring photosynthetic condition of two tank-cultivated red macroalgae using fishpond effluents. Bot. Mar. 2006, 49:275-282.
28. Franklin L.A., Kräbs G., Kuhlenkamp R. Blue light and UV-A radiation control the synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae). J. Phycol. 2001, 37:257-270.
29. Gómez I., Figueroa F.L. Effects of solar UV stress on chlorophyll fluorescence kinetics of intertidal macroalgae from southern Spain: a case study in Gelidium species. J. Appl. Phycol. 1998, 10:285-294.
30. Gómez I., Figueroa F.L., Huovinen P., Ulloa N., Morales V. Photosynthesis of the red alga Gracilaria chilensis under natural solar radiation in an estuary in southern Chile. Aquaculture 2005, 244:369-382.
31. Gómez I., Figueroa F.L., Sousa-Pinto I., Viñegla B., Pérez-Rodríguez E., Maestre C., Coelho S., Felga A., Pereira R. Effects of UV radiation and temperature on photosynthesis as measured by PAM fluorescence in the red alga Gelidium pulchellum (Turner) Kutzing. Bot. Mar. 2001, 44:9-16.
32. Gómez-Pinchetti J.L., del Campo Fernández E., Moreno Díez P., Reina G. Nitrogen availability influences the biochemical composition and photosynthesis of tank-cultivated Ulva rigida (Chlorophyta). J. Appl. Phycol. 1998, 10:383-389.
33. Gómez-Pinchetti, J.L., Suárez álvarez, S., Martel Quintana, A., García Reina, G., 2002. Alternative high-value seaweed species as biofilters for the purification of N-NH4+ enriched fishpond effluents, in: Almería, Servicio de publicaciones de la Universidad de Almería (Ed.), Algal Biotechnology: A Sea of opportunities, Almería.
34. Guiry M.D., Blunden G. Seaweed resources in Europe: Uses and potential, in: Aquatic Conservation: Marine and Freshwater Ecosystems 1992, John Wiley & Sons, Ltd., Chichester, pp. 209-210.
35. Huheihel M., Ishanu V., Tal J., Arad S. Activity of Porphyridium sp polysaccharide against herpes simplex viruses in vitro and in vivo. J. Biochem. Bioph. Meth. 2002, 50:189-200.
36. Huovinen P., Gómez I., Figueroa F.L., Ulloa N., Morales V., Lovengreen C. Ultraviolet-absorbing mycosporine-like amino acids in red macroalgae from Chile. Bot. Mar. 2004, 47:21-29.
37. Huovinen P., Matos J., Pinto I.S., Figueroa F.L. The role of ammonium in photoprotection against high irradiance in the red alga Grateloupia lanceola. Aquat. Bot. 2006, 84:308-316.
38. Jiménez del Rio M., Ramazanov Z., García Reina G. Ulva rigida (Ulvales, Chlorophyta) tank culture as biofilters for dissolved inorganic nitrogen from fishpond effluents. Hydrobiologia 1996, 327:61-66.
39. Jin E., Lee C.G., Polle J.E.W. Secondary carotenoid accumulation in Haematococcus (Chlorophyceae): biosynthesis, regulation, and biotechnology. J. Microbiol. Biotech. 2006, 16:821-831.
40. Korbee N., Figueroa F.L., Aguilera J. 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. Photoch. Photobio. B 2005, 80:71-78.
41. Korbee N., Huovinen P., Figueroa F.L., Aguilera J., Karsten U. Availability of ammonium influences photosynthesis and the accumulation of mycosporine-like amino acids in two Porphyra species (Bangiales, Rhodophyta). Mar. Biol. 2005, 146:645-654.
42. Korbee-Peinado N., Abdala Díaz R.T., Figueroa F.L., Helbling E.W. Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia. Argentina J. Phycol. 2004, 40:248-259.
43. Kräbs G., Watanabe M., Wiencke C. A monochromatic action spectrum for the photoinduction of the UV-absorbing mycosporine-like amino acid shinorine in the red alga Chondrus crispus. Photochem. Photobiol. 2004, 79:515-520.
44. Kroom M.D., Ellner S., van Rijn J., Neori A. Nitrogen and phosphorus cycling and transformations in a prototype 'non-polluting' integrated mariculture system, Eilat. Israel Mar. Ecol. Prog. Ser. 1995, 118:25-36.
45. Lahaye M., Gomez-Pinchetti J.L., del Río M.J., García Reina G. Natural decoloration, composition and increase in dietary fiber content of an edible marine-algae, Ulva rigida (Chlorophyta), grown under different nitrogen conditions. J. Sci. Food Agr. 1995, 68:99-104.
46. Lapointe B.E., Duke C.S. Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light-intensity and nitrogen availability. J. Phycol. 1984, 20:488-495.
47. López-Figueroa F., Niell F.X. Effects of light quality on chlorophyll and biliprotein accumulation in seaweeds. Mar. Biol. 1990, 104:321-327.
48. Luiten E.M., Akkerman I., Koulman A., Kamermans P., Reith H., Barbosa M.J., Sipkema D., Wijffels R.H. Realizing the promises of marine biotechnology. Biomol. Eng. 2003, 20:429-439.
49. Mata, L., Santos, R., 2001. Cultivation of Ulva rotundata (Ulvales, Chlorophyta) in raceways, using semi-intensive fishpond effluents: yield and biofiltration. In: A. R. Chapman, R.J. A, V. J. Vreeland, I. R. Davison (Eds.), 7th International Seaweed Symposium, Oxford University Press, Cape Town.
50. Mata L., Silva J., Schuenhoff A., Santos R. Is the tetrasporophyte of Asparagopsis armata (Bonnemaisoniales) limited by inorganic carbon in integrated aquaculture?. J. Phycol. 2007, 43:1252-1258.
51. Melo M.R.S., Feitosa J.P.A., Freitas A.L.P., de Paula R.C.M. Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohyd. Polym. 2002, 49:491-498.
52. Moigne, J.Y., 1998. Use of algae extracts as antibacterial and/or antifungal agent and composition containing same. In: Borowitzka, M.A. 1999 (Ed.), World Patent 98/10656 Assignee: Algues et Mer. Patents. J. Appl. Phycol. 10, 503-505.
53. Morris-Quevedo H.J., Martínez-Manrique C., Abdala-Díaz R., Cobas-Pupo G. Evidencias preliminares de la actividad inmunomoduladora de la fracción polisacárida de origen marino PC-1. Rev. Cubana Oncol. 2000, 16:171-176.
54. Msuya F., Neori A. Effect of water aeration and nutrient load level on biomass yield, N uptake and protein content of the seaweed Ulva lactuca cultured in seawater tanks. J. Appl. Phycol. 2008, 20:1021-1031.
55. Msuya F.E., Neori A. Ulva reticulata and Gracilaria crassa: Macroalgae that can biofilter effluent from tidal fishponds in Tanzania. Western Indian Ocean J. Mar. Sci 2002, 1:117-126.
56. Nakayama R., Tamura Y., Kikuzaki H., Nakatani N. Antioxidant effect of the constituents of susabinori (Porphyra yezoensis). J. Am. Oil Chem. Soc. 1999, 76:649-653.
57. Neori A., Troellm M., Chopin T., Yarish C., Critchley A., Buschmann A. The need for a balanced ecosystem approach to blue revolution aquaculture. Environment 2007, 49:37-43.
58. Neori A., Msuya F.E., Shauli L., Schuenhoff A., Kopel F., Shpigel M. A novel three-stage seaweed biofilter design for integrated mariculture. J. Appl. Phycol. 2003, 15:543-553.
59. Parsons T.R., Maita Y., Lalli C.M. A Manual of Chemical and Biological Methods for Seawater Analysis 1984, Pergamon Press, Oxford, 173 p.
60. Pereira-Pacheco F., Robledo D., Rodríguez-Carvajal L., Freile-Pelegrín Y. Optimization of native agar extraction from Hydropuntia cornea from Yucatán, México. Bioresour. Technol. 2007, 98:1278-1284.
61. Redfield A.C.B., Ketchum B.H., Richards E.A. The influence of organisms on the composition of seawater. The sea. Interscience 1963, 27-77. M.N. Hill (Ed.).
62. Schreiber U., Endo T., Mi H., Asada K. Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol. 1995, 36:873-882.
63. Schuenhoff A., Mata L., Santos R. The tetrasporophyte of Asparagopsis armata as a novel seaweed biofilter. Aquaculture 2006, 252:3-11.
64. Talarico L., Maranzana G. Light and adaptive responses in red macroalgae: an overview. J. Photochem. Photobiol. 2000, 56:1-11.
65. Tannin-Spitz T., Bergman M., van-Moppes D., Grossman S., Arad S. Antioxidant activity of the polysaccharide of the red microalga Porphyridium sp. J. Appl. Phycol. 2005, 17:215-222.
66. Underwood A.J. Experiments in ecology: their logical design and interpretation using analysis of variance 1997, Cambridge University Press, Cambridge.
67. Vergara J.J., Niell F.X., Torres M. Culture of Gelidium sesquipedale (Clem) born et thur in a chemostat system - biomass production and metabolic responses affected by n-flow. J. Appl. Phycol. 1993, 5:405-415.
68. Werner G.H., Jollès P. Immunostimulating agents: what next?. Eur. J. Biochem. 1996, 242:1-19.
69. Yoshizawa Y. In vivo macrophage-stimulation activity of the enzyme-degraded water-soluble polysaccharide fraction from a marine alga (Gracilaria verrucosa). Biosci. Biotech. Bioch. 1996, 60:1667-1671.