Abstract
Hypnea pseudomusciformis Nauer, Cassano and M.C. Oliveira, a morphologically plastic species used as carrageenan source in Brazil, was recently described based on molecular markers. Two species previously described for the Brazilian coast (H. musciformis (Wulfen) J.V. Lamouroux and H. nigrescens Greville ex J. Agardh) are currently considered morphological variations of H. pseudomusciformis that are found in different intertidal regions. In this work, we investigated whether this morphologically plastic species also present physiological plasticity related to the different morphologies. The content of photosynthetic pigments (chlorophyll a, carotenoids and phycobiliproteins), total soluble proteins and antioxidant capacity (DPPH, ABTS, Folin–Ciocalteu reductive capacity, FRAP and iron chelating capacity) were analyzed for samples of the two morphological variations collected directly from the field or grown in culture. Physiological differences between the two morphological variants from field samples were observed for phycoerythrin, total soluble protein and for all the antioxidant assays, with the exception of DPPH. While between cultured samples, differences were found for phycocyanin, phycoerythrin and total soluble proteins. Overall, the two morphological variants have a similar physiological behavior when grown under the same culture conditions, corroborating its classification under one species. These results indicate that the physiological differences found between these variants are mostly due to environmental pressures and represent an example of phenotypic plasticity, which allows the occurrence of this species in different environments and may lead to different morphologies in the field.
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Aguilera J, Dummermuth A, Karsten U, Schriek R, Wiencke C (2002) Enzymatic defenses against photooxidative stress induced by ultraviolet radiation in Artic marine macroalgae. Polar Biol 25:432–441
Barufi JB, Mata MT, Oliveira MC, Figueroa FL (2012) Nitrate reduces the negative effect of UV radiation on photosynthesis and pigmentation in Gracilaria tenuistipitata (Rhodophyta): the photoprotection role of mycosporine-like amino acids. Phycologia 51:636–648
Benzie I, Strain J (1996) The ferric reducing ability of plasma (FRAP) as a measure of ‘‘antioxidant power’’: the FRAP assay. Anal Bioch 239:70–76
Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28:25–30
Castelo-Branco VN, Torres AG (2011) Capacidade antioxidante total de óleos vegetais comestíveis: determinantes químicos e sua relação com a qualidade dos óleos. Rev Nutr 24:173–187
Choo K-S, Snoeijs P, Pedersén M (2004) Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana. J Exp Mar Biol Ecol 298:111–123
Costa VL, Plastino EM (2011) Color inheritance and pigment characterization of red (wild-type), green strains of Gracilaria birdiae (Gracilariales, Rhodophyta). J Appl Phycol 23:599–605
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 17:205–220
Cunningham FX, Dennenberg RJ, Mustardy L, Jursinic PA, Gantt E (1989) Stoichiometry of photosystem I, photosystem II, and phycobilisomes in the red alga Porphyridium cruentum as a function of growth irradiance. Plant Physiol 91:1179–1187
De la Coba F, Aguilera J, Figueroa FL, De Gálvez MV, Herrera E (2009) Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J Appl Phycol 21:161–169
Faria AV, Plastino EM (2015) Physiological assessment of the mariculture potential of a Gracilaria caudata (Gracilariales, Rhodophyta) variant. J Appl Phycol 28:2445–2452
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Figueroa FL, Salles S, Aguilera J, Jiménez C, Mercado J, Viñegla B, Flores-Moya A, Altamirano M (1997) Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar Ecol Prog Ser 151:81–90
Floegel A, Kim D-O, Chung S-J, Koo SI, Chun OK (2011) Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods. J Food Compos Anal 24:1043–1048
Franklin LA, Forster RM (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32:207–232
Geraldino PJL, Yang EC, Kim MS, Boo SM (2009) Systematics of Hypnea asiatica sp. nov. (Hypneaceae, Rhodophyta) based on morphology and nrDNA SSU, plastid rbcL, and mitochondrial cox1. Taxon 58:606–616
Gómez I, Wulff A, Roleda MY, Huovinen P, Quartino ML, Dunton K, Christian W (2009) Light and temperature demands of marine benthic microalgae and seaweeds in polar regions. Bot Mar 52:593–608
Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122
Guarino AG (2013) Variabilidade e atuação defensiva de polifenóis em macroalgas pardas. Tese de Doutorado. Universidade Federal Fluminense, Rio de Janeiro
Hall TA (1999) BioEdit: a user-friendly biological alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Harb TB, Torres PB, Pires JS, Dos Santos DYAC, Chow F (2016) Ensaio em microplaca do potencial antioxidante através do sistema quelante de metais para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. ISBN 978-85-85658-63-2
Houvinen P, Gómez I (2011) Spectral attenuation of solar radiation in Patagonian fjord and coastal waters and implications for algal photobiology. Cont Shelf Res 31:254–259
Huang HL, Wang BG (2004) Antioxidant capacity and lipophilic content of seaweeds collected from the Qingdao coastline. J Agric Food Chem 52:4993–4997
Kim SJ, Woo S, Yun H, Yum S, Choi E, Do JR, Jo JH, Kim D, Lee S, Lee TK (2005) Total phenolic contentes and biological activities of Korean seaweed extracts. Food Sci Biotechnol 14:798–802
Kiran VM, Murugesan S (2014) Antioxidant activity of silver nano-particles from Colpomenia sinuosa and Halymenia poryphyroids. World J Pharm Sci 2:817–820
Kumar KS, Ganesan K, Rao PVS (2008) Antioxidant potential of solvent extracts of Kappaphycus alvarezii (Doty) Doty—An edible seaweed. Food Chem 107:289–295
Kursar TA, van der Meer JP, Alberte RS (1983) Light harvesting system of the red alga Gracilaria tikvahiae. II. Phycobilisome characteristics of pigment mutants. Plant Physiol 73:361–369
Lamouroux JV (1813) Essai sur les genres de la famille des Thalassiophytes non articulées. Annales du Muséum d’Histoire Naturelle, Paris 20: 21–47, 115–139, 267–293, pls 7–13
Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH (2008) Antioxidant activities and phenolics content of eight species of seaweed from North Borneo. J Appl Phycol 20:367–373
Matsukawa R, Dubinsky Z, Kishimoto E, Masakki K, Masuda Y, Takeuchi TA (1997) comparison of screening methods for antioxidant activity in seaweeds. J Appl Phycol 9:29–35
Min B, McClung AM, Chen M-H (2011) Phytochemicals and antioxidant capacities in rice brans of different color. J Food Sci 76:117–126
Nauer F, Cassano V, Oliveira MC (2015) Description of Hypnea pseudomusciformis sp. nov., a new species based on molecular and morphological analyses, in the context of the H. musciformis complex (Gigartinales, Rhodophyta). J Appl Phycol 27:2405–2417
Pires J, Torres PB, dos Santos DYAC, Chow F (2017a) Ensaio em microplaca do potencial antioxidante através do método de sequestro do radical livre DPPH para extatos de algas. Instituto de Biociências. Universidade de São Paulo, São Paulo. ISBN 978-85-85658-71-7
Pires J, Torres PB, dos Santos DYAC, Chow F (2017b) Ensaio em microplaca de substâncias redutoras pelo método do Folin–Ciocalteudo para extatos de algas. Instituto de Biociências. Universidade de São Paulo, São Paulo. ISBN 978-85-85658-70-0
Plastino EM, Guimarães M (2001) Diversidad intraespecifica. In: Alveal KV, Antezana TJ (eds) Sustentabilidad de la Biodiversidad. Universidad de Concepción, Concepción, pp 19–27
Plastino EM, Ursi S, Fujii MT (2004) Color inheritance, pigment characterization, and growth of a rare light green strain of Gracilaria birdiae (Gracilariales, Rhodophyta). Phycol Res 52:45–52
Rafiquzzaman SM, Ahmad MU, Lee JM, Kim EY, Kim YO, Kim DG, Kong IS (2015) Phytochemical composition and antioxidant activity of edible red alga Hypnea musciformis from Bangladesh. J Food Process Preserv 40:1074–1083
Reis RP, Yoneshigue-Valentin Y (2000) Phenology of Hypnea musciformis (Wulfen) Lamouroux (Rhodophyta, Gigartinales) in three populations from Rio de Janeiro State, Brazil. Bot Mar 43:304
Reis RP, Leal MCR, Yoneshigue-Valentin Y, Belluco F (2003) Efeito de fatores bióticos no crescimento de Hypnea musciformis (Rhodophyta - Gigartinales). Acta Bot Bras 17:279–286
Reis RP, Caldeira AQ, Miranda APS, Barros Barreto MB (2006) Potencial para maricultura da carragenófita Hypnea musciformis (Wulfen) J.V. Lamour. (Giagartinales - Rhodophyta) na Ilha da Marambaia, Rio de Janeiro, Brasil. Acta Bot Bras 20:763–769
Rocha FD, Pereira RC, Kaplan MAC, Teixeira VL (2007) Natural products of marine seaweeds and their antioxidant potential. Rev Bras Farmacogn 17:631–639
Roginsky V, Lissi EA (2005) Review of methods to determine chain-breaking antioxidant activity in food. Food Chem 92:235–254
Rufino MSM, Alves RE, Brito ES, Morais SM, Sampaio CG, Pérez-Jiménez J, Saura-Calixto FD (2006) Metodologia científica: Determinação da atividade antioxidante total em frutas pelo método de redução do ferro (FRAP). Comunicado Técnico, 125 pp
Sabeena Farvin KH, Jacobsen C (2015) Antioxidant activity of seaweed extracts. In vitro assays, evaluation in 5% fish oil-in-water emulsions and characterization. J Am Oil Chem Soc 92:571
Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc B 360:1879–1888
Schenkman RPF (1986) Cultura de Hypnea (Rhodophyta) in vitro como subsídio para estudos morfológicos, reprodutivos e taxonômicos. Instituto de Biociências, Universidade de São Paulo, Tese de Doutorado
Schmidt ÉC, Felix MRL, Kreusch MG, Pereira DT, Costa GB, Simioni C, Ouriques LC, Steiner N, Chow F, Floh ESL, Ramlov F, Maraschin M, Bouzon ZL (2016) Profiles of carotenoids and amino acids and total phenolic compounds of the red alga Pterocladiella capillacea exposed to cadmium and different salinities. J Appl Phycol 28:1955–1963
Sies H (1993) Strategies of antioxidant defence: review. Eur J Biochem 215:213–219
Singleton V, Rossi J (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticul 16:144–158
Swofford DL (2002) PAUP: Phylogenetic Analysis Using Parismony, version 4.08a. Computer program distributed by the Illinois Natural History Survey, Champaign, Ill
Tala F, Chow F (2014) Ecophysiological characteristics of Porphyra spp. (Bangiophyceae, Rhodophyta): seasonal and latitudinal variations in northern-central Chile. J Appl Phycol 26:2159–2171
Torres PB (2012) Análise de pigmentos fotossintetizantes e substâncias fenólicas em Gracilariopsis tenuifrons (C.J. Birdi & E.C. Oliveira) Fredericq & Hommersand em diferentes intensidades de luz. Dissertação de mestrado. Instituto de Biociências, Universidade de São Paulo. 104p
Torres PB, Pires J, dos Santos DYAC, Chow F (2017) Ensaio de potencial antioxidante de extratos de algas através do sequestro do ABTS em microplaca. Instituto de Biociências. Universidade de São Paulo, São Paulo. ISBN 978-85-85658-69-4
Urrea-Victoria V, Pires J, Torres PB, dos Santos DYAC, Chow F (2016) Ensaio antioxidante em microplaca de poder de redução de ferro (FRAP) para extratos de algas. Instituto de Biociências. Universidade de São Paulo, São Paulo. ISBN 978-85-85658-62-5
Ursi S, Plastino EM (2001) Crescimento in vitro de linhagens de coloração vermelha e verde clara de Gracilaria sp. (Gracilariales, Rhodophyta) em dois meios de cultura: análise de diferentes estádios reprodutivos. Rev Bras Bot 4:585–592
Waterman PG, Mole S (1994) Extraction and chemical quantification. In: Waterman PG, Mole S (eds) Analysis of phenolic plant metabolites. Blackwell Scientific Publications, Oxford, pp 83–85
Wu H, Jiang H, Liu C, Deng Y (2015) Growth, pigment composition, chlorophyll fluorescence and antioxidant defenses in the red alga Gracilaria lemaneiformis (Gracilariales, Rhodophyta) under light stress. S Afr J Bot 100:27–32
Yan XJ, Nagata T, Fan X (1998) Antioxidant activities in some common seaweeds. Plant Food Hum Nutr 52:253–262
Yang H, Dong Y, Du H, Shi H, Peng Y, Li X (2011) Antioxidant compounds from propolis collected in Anhui, China. Molecules (Basel, Switzerland) 16:3444–3455
Yokoya NS, Necchi O, Martins AP, Gonzalez SF, Plastino EM (2007) Growth responses and photosynthetic characteristics of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J Appl Phycol 19:197–205
Zubia M, Robledo D (2007) Antioxidant activities in tropical marine macroalgaes from the Yucatan Peninsula, Mexico. J Appl Phycol 19:449–458
Acknowledgements
We are thankful for grateful for Rosário Petti and Willian Oliveira for technical support. Financial support was provided by FAPESP (Biota 2013-11833-3) and CNPq (301491/2013-5).
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FN and MCO conducted field work. FN, AMA and JPS conducted lab work, gathered and analyzed data. MCO and FC supervised the study and contributed to discussion. All authors were involved in writing and discussion of the manuscript.
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Nauer, F., Amorim, A.M., Santos, J.P. et al. Physiological plasticity in morphological variations of red seaweed Hypnea pseudomusciformis (Gigartinales, Rhodophyta) uncovered by molecular, antioxidant capacity and pigments content data. Braz. J. Bot 41, 567–577 (2018). https://doi.org/10.1007/s40415-018-0487-3
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DOI: https://doi.org/10.1007/s40415-018-0487-3