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Ecotypes of Hypnea pseudomusciformis (Cystocloniaceae, Rhodophyta) revealed by physiological, morphological, and molecular data

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Abstract

The red seaweed Hypnea pseudomusciformis has economic potential for mariculture as a source of carrageenan and other products. This work investigates this species along the Brazilian coastline by evaluating the effects of irradiance (40, 70, and 100 μmol photons m−2 s−1) on the number of differentiated branches (Br), growth rates (GR), photosynthesis parameters, and pigment content of tetrasporophytes from five distinct geographical populations extending from 5° to 27° S of latitude. The specimens showed intraspecific divergence for COI-5P marker, divided into three haplotypes with distinct geographical distribution. Although irradiance effects were significant only for GR and Br, intraspecific diversity was significant in all variables analyzed, with the haplotype of the tropical zone (5° to 12° S) displaying higher GR, Br, and maximum quantum yield (Fv/Fm) than the haplotype of the subtropical zone (23° to 27° S), which displayed higher pigment concentration. The geographic intermediate haplotype (19° S) displayed similar GR, Br, and Fv/Fm to the tropical haplotype, but similar pigment content to the subtropical haplotype. Our results indicate the presence of ecotypes within H. pseudomusciformis throughout its geographic distribution. Considering the set of physiological attributes, specimens from the tropical zone have higher potential for mariculture.

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References

  • Ayres-Ostrock LM (2014) Estudos populacionais em Gracilaria birdiae e G. caudata (Gracilariales, Rhodophyta): aspectos fenológicos, fisiológicos e moleculares, Doctoral Thesis, Univ. S. Paulo. São Paulo. 111p.

  • Ayres-Ostrock LM, Valero M, Manger S, Oliveira MC, Plastino EM, Guillemin M, Destombe C (2019) Dual influence of terrestrial and marine historical processes on the phylogeography of the Brazilian intertidal red alga Gracilaria caudata. J Phycol 55:1096–1114

    CAS  PubMed  Google Scholar 

  • Berchez FAS, Pereira RTL, Kamiya NF (1993) Culture of Hypnea musciformis (Rhodophyta, Gigartinales) on artificial substrates attached to linear ropes. Hydrobiologia 260:415–420

    Google Scholar 

  • Breeman AM, Pakker H (1994) Temperature ecotypes in seaweeds: adaptive significance and biogeographic implications. Bot Mar 37:171–180

    Google Scholar 

  • Brunelli B (2017) Filogeografia de Gelidium floridanum e Pterocladiella capillacea (Gelidiales, Rhodophyta) e espécies relacionadas no Atlântico ocidental, com ênfase no Brasil, com base em dados morfológicos e moleculares. Masters Dissertation. Instituto de Botânica de São Paulo. São Paulo. 111p.

  • Castelar B, Reis RP, Azeredo F, Mattos P, Berardinelli G (2016) Hypnea musciformis: alternative or complement to the production of Kappaphycus alvarezii introduced in tropical countries? Aquac Res 47:3538–3550

  • Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17

    Google Scholar 

  • Dyer RJ, Nason JD (2004) Population graphs: the graph theoretic shape of genetic structure. Mol Ecol 13:1713–1727

    PubMed  Google Scholar 

  • Enriquez S, Borowitzka MA (2011) The use of the fluorescence signal in studies of seagrass and macroalgae. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and developments. Springer, Dordrecht, pp 187–208

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    PubMed  Google Scholar 

  • Faria AVF, Bonomi-Barufi J, Plastino EM (2017) Ecotypes of Gracilaria caudata (Gracilariales, Rhodophyta): physiological and morphological approaches considering life history phases. J Appl Phycol 29:707–719

    CAS  Google Scholar 

  • Fernandes DRP, Caetano VS, Tenório MMB, Reinert F, Yoneshigue-Valentin Y (2012) Characterization of the photosynthetic conditions and pigment profiles of the colour strains of Hypnea musciformis from field-collected and in vitro cultured samples. Rev Bras Farmacogn 22:753–759

    CAS  Google Scholar 

  • Gantt E (1990) Pigmentation and photoacclimation. In: Cole KM, Sheath RG (eds) Biology of the Red Algae. Cambridge University Press, Cambridge pp 203–219.

  • Gomes da Silva P, Dalinghaus C, González M, Gutiérrez Gutiérrez O, Espejo A, Abascal A, Klein AH (2015) Estimating flooding level through the Brazilian Coast using reanalysis data. J Coast Res 75:1092–1096

    Google Scholar 

  • Guimaraens MA, Coutinho R (2000) Temporal and spatial variation of Ulva spp. and water properties in the Cabo Frio upwelling region of Brazil. Aquat Bot 66:101–114

    Google Scholar 

  • Horta PA, Amancio E, Coimbra CS, Oliveira EC (2001) Consideracções sobre a distribuição e origem da flora de macroalgas marinhas Brasileiras. Hoehnea 28:243–265

    Google Scholar 

  • Jesus PB, Costa AL, Nunes JMC, Manghisi A, Genovese G, Morabito M, Schnadelbach AS (2019) Species delimitation methods reveal cryptic diversity in the Hypnea cornuta complex (Cystocloniaceae, Rhodophyta). Eur J Phycol 54:135–153

    Google Scholar 

  • Karsten U, West JA, Zuccarello G, Kirst GO (1994) Physiological ecotypes in the marine alga Bostrychia radicans (Ceramiales, Rhodophyta) from the east coast of the U.S.A. J Phycol 30:174–182

    Google Scholar 

  • Kirk JTO (1994) Light & photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge

    Google Scholar 

  • Kromkamp JC, Forster RM (2003) Review – The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112

    Google Scholar 

  • Kursar TA, Van Der Meer J, Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analyses of pigment mutations. Plant Physiol 73:353–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lobban CS, Harrison P (1994) Light and photosynthesis. In: Seaweed ecology and physiology. Cambridge University Press, Cambridge, pp 123–159

    Google Scholar 

  • Lowry DB (2012) Ecotypes and the controversy over stages in the formation of new species. Biol J Linn Soc 106:241–257

    Google Scholar 

  • Marchi F, Plastino EM (2020) Codominant inheritance of polymorphic color mutant and characterization of a bisexual mutant of Gracilaria caudata (Gracilariales, Rhodophyta). J App Phycol https://doi.org/10.1007/S10811-020-02199-W

  • 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

    CAS  Google Scholar 

  • Nauer F, Jesus PB, Cassano V, Nunes JMC, Schnadelbach AS, Oliveira MC (2019a) A taxonomic review of the genus Hypnea (Gigartinales, Rhodophyta) in Brazil based on DNA barcode and morphology. Braz J Bot 42:561–574

    Google Scholar 

  • Nauer F, Deluqui Gurgel CF, Ayres-Ostrock LM, Plastino EM, Oliveira MC (2019b) Phylogeography of the Hypnea musciformis species complex (Gigartinales, Rhodophyta) with the recognition of cryptic species in the western Atlantic Ocean. J Phycol 55:676–687

    CAS  PubMed  Google Scholar 

  • Novaczek I, Lubbers GW, Breeman AM (1990) Thermal ecotypes in amphi-Atlantic algae. I. Algae of Arctic to cold-temperate distribution (Chaetomorpha melagonium, Devaleraea ramentacea and Phycodrys rubens). Helgol Meeresunters 44:459–474

    Google Scholar 

  • Novembre J, Stephens M (2008) Interpreting principal component analyses of spatial population genetic variation. Nat Genet 40:646–649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oppliger LV, Correa JA, Engelen AH, Tellier F, Vieira V, Faugeron S, Valero M, Gomez G, Destombe C (2012) Temperature effects on gametophyte life-history traits and geographic distribution of two cryptic kelp species. PLoS One 7:e39289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Orfanidis S (1992) Light requirements for growth in six shade-acclimated Mediterranean macroalgae. Mar Biol 112:511–515

    Google Scholar 

  • Orfanidis S, Venekamp LAH, Breeman A (1999) Ecophysiological adaptations of two Mediterranean red algae in relation to distribution. Eur J Phycol 34:469–476

    Google Scholar 

  • Pereira SA, Kimpara JM, Valenti WC (2020) A simple substrate to produce the tropical epiphytic algae Hypnea pseudomusciformis. Aquacult Eng 89:102066

    Google Scholar 

  • Plastino EM, Guimarães M (2001) Diversidade intraespecífica. In: Alveal K, Antezana T (eds) Sustentabilidad de la biodiversidad, un problema actual. Bases cientifico-tecnicas, teorizaciones y proyecciones. Universidad de Concepción 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

    Google Scholar 

  • Prates AP, Henrique De Lima L, Chatwin A (2007) Coastal and marine conservation priorities in Brazil. Priorities for coastal and marine conservation in South America. The Nature Conservancy, Arlington Virginia. USA pp 15–23.

  • Reis RP, Leal MCR, Yoneshigue-Valentin Y, Belluco R (2003) Efeito de fatores bióticos no crescimento de Hypnea musciformis (Rhodophyta - Gigartinales). Acta Bot Bras 17:279–286

    Google Scholar 

  • Reis RP, Caldeira AQ, Miranda APS, Barros-Barreto MB (2006) Potencial para maricultura da carragenófta Hypnea musciformis (Wulfen) J.V. Lamour. (Gigartinales - Rhodophyta) na Ilha da Marambaia, Baía de Sepetiba, RJ, Brasil. Acta Bot Bras 20:763–769

    Google Scholar 

  • Ribeiro ALNL, Chiozzini VG, Braga ES, Yokoya NS (2017) Physiological responses and biofilter potential of Hypnea aspera (Rhodophyta, Gigartinales) cultivated in different availabilities of nitrate, ammonium, and phosphate. J Appl Phycol 29:683–694

    CAS  Google Scholar 

  • Rietema H (1991) Evidence for ecotypic divergence between Phycodrys rubens populations from the Baltic Sea and North Sea. Bot Mar 34:375–381

    Google Scholar 

  • Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Talarico L (1996) Phycobiliproteins and phycobilisomes in red algae: adaptive responses to light. Sci Mar 60:205–222

    CAS  Google Scholar 

  • Thiers B (2020) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://www.nybg.org/bsci/ih/ih.html. [continuously updated].

  • Ursi S, Plastino EM (2001) Crescimento in vitro de linhagens de coloração vermelha e verde clara de Gracilaria birdiae (Gracilariales, Rhodophyta) em dois meios de cultura: análise de diferentes estádios reprodutivos. Rev Bras Bot 24:587–594

    Google Scholar 

  • Ursi S, Pedersén M, Plastino EM, Snoeijs P (2003) Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Mar Biol 142:997–1007

    CAS  Google Scholar 

  • Van den Hoek C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, Cambridge

    Google Scholar 

  • Yokoya NS, Oliveira EC (1992a) Temperature responses of economically important red algae and their potential for mariculture in Brazilian waters. J Appl Phycol 4:339–345

    Google Scholar 

  • Yokoya NS, Oliveira EC (1992b) Effects of salinity on the growth rate, morphology and water content of some Brazilian red algae of economic importance. Cienc Mar 18:49–64

    CAS  Google Scholar 

  • Yokoya YS, Necchi O Jr, 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

    CAS  Google Scholar 

  • Yong YS, Yong WTL, Anton A (2013) Analysis of formulae for determination of seaweed growth rate. J Appl Phycol 25:1831–1834

    Google Scholar 

  • Zubia M, Olivier P, Thomas OP, Soulet S, Demoy-Schneider M, Saulnier D, Connan S, Murphy EC, Tintillier F, Stiger-Pouvreau V, Petek S (2019) Potential of tropical macroalgae from French Polynesia for biotechnological applications. J Appl Phycol 32:2343–2362

    Google Scholar 

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Funding

This study was funded by grants from FAPESP (2018/11445-7, 2019/08734-0). We thank Rosário Petti and Vivian Viana for technical support. MCO, MTF, and EMP thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Productivity Fellowship (305687/2018-2, 304899/2017-8, and 300148/93-3, respectively). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

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Authors and Affiliations

  1. Nucleus for Research in Phycology, Institute of Botany, Av. Miguel Estéfano 3687, São Paulo, 04301-902, Brazil

    Fabio Nauer & Mutue Toyota Fujii

  2. Department of Botany, Institute of Biosciences, University of São Paulo, Rua do Matão, 277, São Paulo, 05508-090, Brazil

    Matheus Naves, Estela Maria Plastino & Mariana Cabral Oliveira

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  1. Fabio Nauer
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Correspondence to Fabio Nauer.

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Nauer, F., Naves, M., Plastino, E.M. et al. Ecotypes of Hypnea pseudomusciformis (Cystocloniaceae, Rhodophyta) revealed by physiological, morphological, and molecular data. J Appl Phycol 32, 4399–4409 (2020). https://doi.org/10.1007/s10811-020-02267-1

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