Carotenoid content in Ulva lactuca cultivated under aquaculture conditions and collected from intertidal beds in southeastern Brazil: biotechnological implications for biomass use and storage
Article Sidebar
Main Article Content
Abstract
Ulva lactuca is an edible green macroalga (Chlorophyta) that can be produced in cultivation systems; it is a natural source of high-value molecules. Ulva lactuca produces metabolites including carotenoids, which are pigments with antioxidant properties that are in high demand in the health and nutraceutical industries and improve the nutritional quality of U. lactuca biomass. We studied the carotenoid and chlorophyll content in U. lactuca thalli collected in 3 different environments in the state of Rio de Janeiro, Brazil: the intertidal beds of the urban beaches of Arpoador and Boa Viagem and a continental integrated multi-trophic aquaculture (IMTA) facility. Carotenoid conservation was evaluated during 1 week, 2 weeks, and 4 weeks of storage. We compared the molecules in fresh U. lactuca collected during the dry season (July 2018) and rainy season (February 2019). The content of carotenoids, such as β-carotene + zeaxanthin, lutein + antheraxanthin, violaxanthin, neoxanthin, and their derivatives (aurochrome and auroxanthin), were analyzed in 100% acetone extracts by ultraviolet visible (UV/vis) spectrophotometry and monitored by thin layer chromatography (TLC) and proton nuclear magnetic resonance (1H-NMR). The extracts of dried U. lactuca produced in the IMTA facility presented higher pigment yields than the dried biomass collected from intertidal beds. Over 4 weeks of storage, carotenoids were well conserved in U. lactuca produced in the IMTA facility, in contrast to what was observed in U. lactuca collected from the intertidal beds, which showed carotenoid losses. In addition, we observed differences in carotenoid content between the dry and rainy seasons in U. lactuca collected from Boa Viagem Beach. However, the U. lactuca collected from Arpoador Beach or produced by the IMTA facility only exhibited significant differences in chlorophyll content. We conclude that U. lactuca produced by the IMTA facility constitutes a potential source of pigments such as β-carotene, lutein, and violaxanthin.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
This is an open access article distributed under a Creative Commons Attribution 4.0 License, which allows you to share and adapt the work, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Figures, tables and other elements in the article are included in the article’s CC BY 4.0 license, unless otherwise indicated. The journal title is protected by copyrights and not subject to this license. Full license deed can be viewed here.
Metrics
References
Alves A, Sousa RA, Reis RL. 2013. A practical perspective on ulvan extracted from green algae. J Appl Phycol. 25:407-424. https://doi.org/10.1007/s10811-012-9875-4
Bergquist SÅ, Gertsson UE, Olsson UE. 2006. Influence of growth stage and postharvest storage on ascorbic acid and carotenoid content and visual quality of baby spinach (Spinacia oleracea L.). J Sci Food Agric. 86:346-355. https://doi.org/10.1002/jsfa.2373
Calheiros AC, Sales LPM, Pereira Netto AD, Cavalcanti DN, Castelar B, Reis RP. 2021. Commercial raw materials from algaculture and natural stocks of Ulva spp. J Appl Phycol. 33:1805-1818. https://doi.org/10.1007/s10811-021-02413-3
Carneiro MER, Marques AN, Pereira RC, Cabral MM, Teixeira VL. 2022. Estudos populacionais de Ulva fasciata Delile, indicadora de poluição na Baía da Guanabara. Rev Nerítica. 2:201-211. http://dx.doi.org/10.5380/rn.v2i0.84966
Chakraborty K, Paulraj R. 2010. Sesquiterpenoids with free-radical-scavenging properties from marine macroalga Ulva fasciata Delile. Food Chem. 122:31-41. https://doi.org/10.1016/j.foodchem.2010.02.012
Cruces E, Rautenberger R, Cubillos VM, Ramírez‐Kushel E, Rojas‐Lillo Y, Lara C, Montory JA, Gómez I. 2019. Interaction of photoprotective and acclimation mechanisms in Ulva rigida (Chlorophyta) in response to diurnal changes in solar radiation in southern Chile. J Phycol. 55:1011-1027. https://doi.org/10.1111/jpy.12894
Demmig-Adams B. 1998. Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol. 39:474-482. https://doi.org/10.1093/oxfordjournals.pcp.a029394
Demmig-Adams B, Adams WW. 1996. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1:21-26. https://doi.org/10.1016/S1360-1385(96)80019-7
Derner RB. 2018. Cultivo de macroalgas no Brasil: Potencial desperdiçado. Aquacult Brasil. 12:54-55.
Eismann AI, Reis RP, da Silva AF, Cavalcanti DN. 2020. Ulva spp. carotenoids: Responses to environmental conditions. Algal Res. 48:101916. https://doi.org/10.1016/j.algal.2020.101916
El-Baky HHA, El Baz FK, El-Baroty GS. 2008. Evaluation of marine alga Ulva lactuca L. as a source of natural preservative ingredient. Am Eurasian J Agric Environ Sci. 3(3):434-444. https://idosi.org/aejaes/jaes3(3)/21.pdf
El-Baky HHA, El Baz FK, El-Baroty GS. 2009. Natural preservative ingredient from marine alga Ulva lactuca L. Int J Food Sci Technol. 44:1688-1695. https://doi.org/10.1111/j.1365-2621.2009.01926.x
Esteban R, Barrutia O, Artetxe U, Fernández-Marín B, Hernández A, García-Plazaola JI. 2015. Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. New Phytol. 206:268-280. https://doi.org/10.1111/nph.13186
Esteban R, Fleta-Soriano E, Buezo J, Míguez F, Becerril JC, García-Plazaola JI. 2014. Enhancement of zeaxanthin in two-steps by environmental stress induction in rocket and spinach. Food Res Int. 65:207-214. https://doi.org/10.1016/j.foodres.2014.05.044
Figueroa FL, Nygård C, Ekelund N, Gómez I. 2003. Photobiological characteristics and photosynthetic UV responses in two Ulva species (Chlorophyta) from southern Spain. J Photochem Photobiol Biol. 72:35-44. https://doi.org/10.1016/j.jphotobiol.2003.09.002
Fort A, Lebrault M, Allaire M, Esteves-Ferreira AA, McHale M, Lopez F, Fariñas-Franco JM, Alseekh S, Fernie AR, Sulpice R. 2019. Extensive variations in diurnal growth patterns and metabolism among Ulva spp. strains. Plant Physiol. 180:109-123. https://doi.org/10.1104/pp.18.01513
Fulmer GR, Miller AJ, Sherden NH, Gottlieb HE, Nudelman A, Stoltz BM, Goldberg KI. 2010. NMR chemical shifts of trace impurities: common laboratory solvents, organics, and gasses in deuterated solvents relevant to the organometallic chemist. Organometallics. 29:2176-2179. https://doi.org/10.1021/om100106e
Gateau H, Solymosi K, Marchan J, Schoefs B. 2017. Carotenoids of microalgae used in food industry and medicine. Mini-Rev Med Chem. 17:1140-1172. https://doi.org/10.2174/1389557516666160808123841
Goldman M, Horev B, Saguy I. 1983. Decolorization of β‐carotene in model systems simulating dehydrated foods: Mechanism and kinetic principles. J Food Sci. 48:751-754. https://doi.org/10.1111/j.1365-2621.1983.tb14890.x
Guadagno CR, Della Greca M, de Santo AV, Ambrosio ND. 2013. NMR (1H) analyses of crude extracts detects light stress in Beta vulgaris and Spinacia oleracea leaves. Photosyn Res. 115:115-122. https://doi.org/10.1007/s11120-013-9833-2
Guiry MD, Guiry GM. 2024. AlgaeBase World-Wide Electronic Publication: National University of Ireland; [accessed 2024 May 24]. http://www.algaebase.org.
He Y, Ma Y, Du Y, Shen S. 2018. Differential gene expression for carotenoid biosynthesis in a green alga Ulva prolifera based on transcriptome analyses. BMC Genomics. 19(1):1-14. https://doi.org/10.1186/s12864-018-5337-y
Henley WJ, Ramus R. 1989. Optimization of pigment content and the limits of photoacclimation for Ulva rotundata (Chlorophyta). Mar Biol. 103:267-274. https://doi.org/10.1007/BF00543357
Irwandi J, Noviendri D, Hasrini RS, Octavianti F. 2011. Carotenoids: sources, medicinal properties and their application in food and nutraceutical industry. J Med Plants Res. 5:7119-7131. http://doi.org/10.5897/JMPRx11.011
Jiang H, Gong J, Lou W, Zou D. 2019. Photosynthetic behaviors in response to intertidal zone and algal mat density in Ulva lactuca (Chlorophyta) along the coast of Nan’ao island, Shantou, China. Environ Sci Pollut Res. 26:13346-13353. http://doi.org/10.1007/s11356-019-04775-1
Küpper H, Seibert S, Parameswaran A. 2007. Fast, sensitive, and inexpensive alternative to analytical pigment HPLC: quantification of chlorophylls and carotenoids in crude extracts by fitting with Gauss peak spectra. Anal Chem. 79:7611-7627. https://doi.org/10.1021/ac070236m
Lashbroke JG, Young PR, Strever AE, Stander C, Vivier MA. 2010. The development of a method for the extraction of carotenoids and chlorophylls from grapevine leaves and berries for HPLC profiling. Aust J Grape Wine Res. 16:349-360. https://doi.org/10.1111/j.1755-0238.2010.00097.x
Maoka T. 2020. Carotenoids as natural functional pigments. J Nat Med. 74(1):1-16. https://doi.org/10.1007/s11418-019-01364-x
Meléndez-Martínez AJ, Mandić AI, Bantis F, Böhm V, Borge GIA, Brnčić M, Pilar M, Cano DMG, Elgersma A, Fikselová M, et al. 2022. A comprehensive review on carotenoids in foods and feeds: Status quo, applications, patents, and research needs. Crit Rev Food Sci Nutr. 62:1999-2049. https://doi.org/10.1080/10408398.2020.1867959
Melo NSM, Cardoso LG, de Nunes JM, Brito GB, Caires TA, de Souza CO, Druzian JI. 2021. Effects of dry and rainy seasons on the chemical composition of Ulva fasciata, Crassiphycus corneus, and Sargassum vulgare seaweeds in tropical environment. Braz J Bot. 44:331-344. https://doi.org/10.1007/s40415-021-00700-4
Mikami K, Hosokawa M. 2013. Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int J Mol Sci. 14.7:13763-1378. https://doi.org/10.3390/ijms140713763
Nardelli AE, Chiozzini VG, Braga ES, Chow F. 2019. Integrated multi-trophic farming system between the green seaweed Ulva lactuca, mussel, and fish: a production and bioremediation solution. J Appl Phycol. 31:847-856. https://doi.org/10.1007/s10811-018-1581-4
Narrain D, Baulroop J, Bhagooli R, Bahorun T. 2023. Differential photosynthetic, phytochemical and antioxidative responses of three macroalgae Ulva lactuca, Gracilaria salicornia and Turbinaria ornata exposed to thermal and irradiance conditions. Indo Pac J Ocean Life. 7(1): 1-15. https://doi.org/10.13057/oceanlife/o070101
Obando JMC, dos Santos TC, Martins RCC, Teixeira VL, Barbarino E, Cavalcanti DN. 2022. Current and promising applications of seaweed culture in laboratory conditions. Aquaculture. 560(15):738596. https://doi.org/10.1016/j.aquaculture.2022.738596
Oliveira Soares R, Castelar B, Pontes MD. 2022. Effect of biofilter storage density on the nutrient filtration capacity of Ulva lactuca = Efeito da densidade de estocagem do biofiltro na capacidade de filtração de nutrientes da Ulva lactuca. Res Soc Dev. 11(3):e14111326173. https://doi.org/10.33448/rsd-v11i3.26173
Ortiz J, Romero N, Robert P, Araya J, Lopez- Hernández J, Bozzo C, Navarrete E, Osorio A, Rios A. 2006. Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem. 99(1):98-104. https://doi.org/10.1016/j.foodchem.2005.07.027
Osuna-Ruiz I, Nieves-Soto M, Manzano-Sarabia MM, Hernández-Garibay E, Lizardi-Mendoza J, Burgos-Hernández A, Hurtado-Oliva MÁ. 2019. Gross chemical composition, fatty acids, sterols, and pigments in tropical seaweed species off Sinaloa, Mexico = Composición proximal, ácidos grasos, esteroles y pigmentos en especies tropicales de algas marinas frente a Sinaloa, México. Cienc Mar. 45(3):101-120. https://doi.org/10.7773/cm.v45i3.2974
Pérez-Gálvez A, Mínguez-Mosquera MI. 2001. Structure-reactivity relationship in the oxidation of carotenoid pigments of the pepper (Capsicum annuum L.). J Agric Food Chem. 49:4864-4869. https://doi.org/10.1021/jf010547c
Perucka I, Oleszek W. 2000. Extraction and determination of capsaicinoids in fruit of hot pepper Capsicum annuum L. by spectrophotometry and high-performance liquid chromatography. Food Chem. 71:287-291. https://doi.org/10.1016/S0308-8146(00)00153-9
Pitta JP, Pontes MD, Castelar B, Hamacher C. 2022. Desempenho de curto prazo de Ulva fasciata produzida em diferentes densidades em Aquicultura multitrófica integrada. Conjecturas. 22(9):1-17. https://doi.org/10.53660/CONJ-1385-AG05
Putzbach K, Krucker M, Albert K, Grusak MA, Tang G, Dolnikowski GG. 2005. Structure determination of partially deuterated carotenoids from intrinsically labeled vegetables by HPLC-MS and 1H-NMR. J Agric Food Chem. 53:671-677. https://doi.org/10.1021/jf0487506
Ratnayake R, Liu Y, Paul VJ, Luesch H. 2013. Cultivated sea lettuce is a multiorgan protector from oxidative and inflammatory stress by enhancing the endogenous antioxidant defense system. Cancer Prev Res. 6:989-999. https://doi.org/10.1158/1940-6207.CAPR-13-0014
Raymundo MDS, Horta P, Fett R. 2004. Atividade antioxidante in vitro de extratos de algumas algas verdes (Chlorophyta) do litoral catarinense (Brasil). Rev Bras Cie. Farm. 40:495-503. https://doi.org/10.1590/S1516-93322004000400007
Reis RP, Castelar B, dos Santos AA. 2017. Why is algaculture still incipient in Brazil? J Appl Phycol. 29:673-682. https://doi.org/10.1007/s10811-016-0890-8
Rodriguez-Amaya DB. 2001. A Guide to Carotenoid Analyses in Foods. Washington D.C. (USA): ILSI Press. 60 p.
Roleda MY, Lage S, Aluwini DF, Rebours C, Brurberg MB, Nitschke U, Gentili FG. 2021. Chemical profiling of the Arctic sea lettuce Ulva lactuca (Chlorophyta) mass-cultivated on land under controlled conditions for food applications. Food Chem. 341:127999. https://doi.org/10.1016/j.foodchem.2020.127999
Ryckebosch E, Muylaert K, Eeckhout M, Ruyssen T, Foubert I. 2011. Influence of drying and storage on lipid and carotenoid stability of the microalga Phaeodactylum tricornutum. J Agric Food Chem. 59(20):11063-11069. https://doi.org/10.1021/jf2025456
Safafar H, Langvad S, Møller P, Jacobsen C. 2017. Storage conditions affect oxidative stability and nutritional composition of freeze‐dried Nannochloropsis salina. Eur J Lipid Sci Tech. 119(12):1600477. https://doi.org/10.1002/ejlt.201600477
Sajilata MG, Singhal RS, Kamat MY. 2008. The carotenoid pigment zeaxanthin: a review. Compr Rev Food Sci Food Saf. 7(1):29-49. https://doi.org/10.1111/j.1541-4337.2007.00028.x
Santos TC, Vale TM, Cavalcanti DN, Machado LP, Barbarino E, Martins RC, Obando JM. 2023a. Metabólitos Bioativos e Aplicações Biotecnológicas de Macroalgas do Gênero Sargassum: Uma Revisão. Rev Virtual Quim. 15(4):741-758. http://dx.doi.org/10.21577/1984-6835.20220125
Santos TC, Obando JMC, Cavalcanti DN, Martins RCC. 2023b. Produtos naturais de algas marinhas pertencentes à família Dictyotaceae: potenciais bioativos antifúngico e antioxidante. Biodiversidade. 22(3):55-78. https://periodicoscientificos.ufmt.br/ojs/index.php/biodiversidade/article/view/16386
Santos TC, Obando JMC, Martins RCC, Alves MA, Villaça RC, Machado LP, Gasparoto MCG, Cavalcanti DN. 2024. Chemical Profile by UPLC-HRMS and Antifungal and Antioxidant Activity of Marine Macroalgae Dictyota menstrualis. Rev Virtual Quim. 16(1):1-12. http://dx.doi.org/10.21577/1984-6835.20230044
Sherma J, Fried B. 2003. Handbook of Thin-Layer Chromatography. New York (USA): CRC Press. 1048 p.
Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seixas F, Rema P. 2015. Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology. J Appl Phycol. 27:1671-1680. https://doi.org/10.1007/s10811-014-0453-9
Sivathanu B, Palaniswamy S. 2012. Purification and characterization of carotenoids from green algae Chlorococcum humicola by HPLC-NMR and LC-MS-APCI. Biomed Prev Nutr. 2(4):276-282. https://doi.org/10.1016/j.bionut.2012.04.006
Sobolev AP, Brosio E, Gianferri R, Segre AL. 2005. Metabolic profile of lettuce leaves by high field NMR spectra. Magn Reson Chem. 43(8):625-638. https://doi.org/10.1002/mrc.1618
Sousa MBD, Pires KMDS, Alencar DBD, Sampaio AH, Saker-Sampaio S. 2008. α- and β-carotene and α-tocopherol in fresh seaweed. Food Sci Tech. 28(4):953-958. https://doi.org/10.1590/S0101-20612008000400030
Sugumaran R, Padam BS, Yong WTL, Saallah S, Ahmed K, Yusof NA. 2022. A Retrospective Review of Global Commercial Seaweed Production-Current Challenges, Biosecurity and Mitigation Measures and Prospects. Int J Environ Res Public Health. 19(12):7087. http://doi.org/10.3390/ijerph19127087
Thayer SS, Björkman O. 1990. Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res. 23:331-343. https://doi.org/10.1007/BF00034864
Uribe E, Vega-Gálvez A, García A, Pastén A, López J, Goñi G. 2018. Effect of different drying methods on phytochemical content and amino acid and fatty acid profiles of the green seaweed Ulva spp. J Appl Phycol. 31:1967-1979. https://doi.org/10.1007/s10811-018-1686-9
Valverde J, This H. 2007. 1H-NMR quantitative determination of photosynthetic pigments from green beans (Phaseolus vulgaris L.). J Agric Food Chem. 56(1):314-320. https://doi.org/10.1021/jf070277j
Woodall AA, Lee SWM, Weesie RJ, Jackson MJ, Britton G. 1997. Oxidation of carotenoids by free radicals: relationship between structure and reactivity. Biochim Biophys Acta Gen Subj. 1336:33-42. https://doi.org/10.1016/S0304-4165(97)00006-8
Wright SW, Jeffrey SW, Mantoura RFC. 1997. Evaluation of methods and solvents for pigment extraction. In: Jeffrey SW, Mantoura RFC, Wright SW. (eds.), Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods. Paris (France): UNESCO Publishing. p. 261-283. https://unesdoc.unesco.org/ark:/48223/pf0000105485
Zhang X, Mou S, Cao S, Fan X, Yu D, Ye N. 2015. Roles of the transthylakoid proton gradient and xanthophyll cycle in the non-photochemical quenching of the green alga Ulva linza. Estuar Coast Shelf Sci. 163:69-74. https://doi.org/10.1016/j.ecss.2014.09.006