Morphological and molecular characterization of Udotea species (Bryopsidales, Chlorophyta) from northeastern Brazil with a new record of U. dotyi from the western south Atlantic

MAYARA C. B. S. ROCHA; SONIA M. B. PEREIRA; MARIA F. OLIVEIRA-CARVALHO; ANA M. BENKO-ISEPPON; CAROLINE F. XIMENES; MUTUE T. FUJII; VALÉRIA CASSANO

doi:10.11646/phytotaxa.578.1.3

Issue: Vol. 578 No. 1: 4 January 2023

Type: Article

Published: 2023-01-04

DOI: 10.11646/phytotaxa.578.1.3

Page range: 57-74

Abstract views: 89

PDF downloaded: 7

**Morphological and molecular characterization of Udotea species (Bryopsidales, Chlorophyta) from northeastern Brazil with a new record of U. dotyi from the western south Atlantic**

MAYARA C. B. S. ROCHA⁺⁻
SONIA M. B. PEREIRA⁺⁻
MARIA F. OLIVEIRA-CARVALHO⁺⁻
ANA M. BENKO-ISEPPON⁺⁻
CAROLINE F. XIMENES⁺⁻
MUTUE T. FUJII⁺⁻
VALÉRIA CASSANO⁺⁻

Post-graduate Programme “Biodiversidade Vegetal e Meio Ambiente”, Instituto de Pesquisas Ambientais, Av. Miguel Estefno, 3687, Água Funda, 04301-012 - São Paulo, SP - Brazil

Departamento de Biologia, Universidade Federal Rural de Pernambuco, 52171-900, Recife, Pernambuco - Brazil

Departamento de Genética, Universidade Federal de Pernambuco, 1235, 50670-901, Recife, Pernambuco - Brazil

Departamento de Biologia, Universidade Federal Rural de Pernambuco, 52171-900, Recife, Pernambuco - Brazil

Post-graduate Programme “Biodiversidade Vegetal e Meio Ambiente”, Instituto de Pesquisas Ambientais, Av. Miguel Estefno, 3687, Água Funda, 04301-012 - São Paulo, SP - Brazil

Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP - Brazil

Barcode green algae rbcL taxonomy tufA Algae

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Abstract

Udotea is an exclusively marine green macroalgal genus with wide distribution in both tropical and subtropical regions. Due to the difficulty in properly delimiting infrageneric taxa based on morpho-anatomical characteristics by the presence of cryptic species and phenotypic plasticity, the use of techniques of DNA barcode and phylogenetic analysis have been fundamental to assess the Udotea species diversity. Information concerning this genus in Brazil is currently restricted to a few publications in checklists and/or regional floristic surveys along the tropical coast. This study aimed to evaluate the diversity of Udotea in northeastern Brazil through morphological-based taxonomy allied with plastid molecular markers, tufA and rbcL. We generated phylogenies of Udotea sensu lato, and we used different species delimitation methods to assess the diversity among sequences of selected tufA clades within Udotea sensu stricto. None of the eight infrageneric taxa reported for Brazil based only on morphology were confirmed by using molecular data. Udotea dotyi was revealed by tufA and rbcL sequences and represents its first occurrence for the western south Atlantic Ocean. A taxon named here as ‘Udotea cyathiformis’ requires further studies for its definition. This first molecular study on Udotea from the Brazilian coast shows that a broader sampling will be necessary to assess the true diversity of the genus in the western south Atlantic, which may be overestimated due to its high morphological plasticity.

References

Acosta-Calderón, J.A., Hernández-Rodríguez, C., Mendoza-González, A.C. & Mateo-Cid, L.E. (2018) Diversity and distribution of Udotea genus J.V. Lamouroux (Chlorophyta, Udoteaceae) in the Yucatan peninsula littoral, Mexico. Phytotaxa 345: 179–218. https://doi.org/10.11646/phytotaxa.345.3.1
Barata, D. (2004) Clorofíceas Marinhas Bentônicas do Estado do Espírito Santo. Instituto de Botânica da Secretaria de Estado do Meio Ambiente, São Paulo. 210 pp.
Bouckaert, R., Vaughan, T.G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., DeMaio, N., Matschiner, M., Mendes, F.K., Müller, N.F., Ogilvie, H.A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, C.-H., Xie, D., Zhang, C., Stadler, T. & Drummond, A.J. (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15, e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Clifton, K.E. & Clifton, L.M. (1999) The Phenology Of Sexual Reproduction By Green Algae (Bryopsidales) On Caribbean Coral Reefs. Journal of Phycology 35: 24–34. https://doi.org/10.1046/j.1529-8817.1999.3510024.x
Collado-Vides, L., Suárez, M.A., Cabrera, R. (2009) Una Revisión Taxonomica Del Gênero Udotea em el Caribe Mexicano y Cubano. Revista Investigaciones Marinas 30: 145–61. 
Coppejans, E., Leliaert, F., Verbruggen, H., Prathep, A. & De Clerck, O. (2011) Rhipidosiphon lewmanomontiae sp. nov. (Bryopsidales, Chlorophyta), a calcified udoteacean alga from the central Indo-Pacific based on morphological and molecular investigations. Phycologia 50: 403–412. https://doi.org/10.2216/10-90.1
Curtis, N., Dawes, C. & Pierce, S. (2008) Phylogenetic analysis of the large subunit rubisco gene supports the exclusion of Avrainvillea and Cladocephalus from the Udoteaceae (Bryopsidales, Chlorophyta). Journal of Phycology 44: 761–767. https://doi.org/10.1111/j.1529-8817.2008.00519.x
Dantas, N.P. (1994) Estudos taxonômicos dos representantes da ordem Caulerpales (Chlorophyta) da Praia de Guarajiru (Estado do Ceará- Brasil). Universidade Federal de Pernambuco, Recife, 128 pp. 
DeWreede, R. (2006) Biomechanical properties of coenocytic algae (Chlorophyta, Caulerpales). Science Asia 1: 57–62. https://doi.org/10.2306/scienceasia1513-1874.2006.32(s1).057
Doyle, J.L. & Doyle, J.J. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
Ellis, J. & Solander, D. (1786) The natural history of many curious and uncommon zoophytes. B White & Son London XII: 208. https://doi.org/10.5962/bhl.title.64985
Famà, P., Wysor, B., Kooistra, W.H.C.F. & Zuccarello, G.C. (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. Journal of Phycology 38: 1040–1050. https://doi.org/10.1046/j.1529-8817.2002.t01-1-01237.x
Fenical, W. & Paul, V.J. (1984) Antimicrobial and cytotoxic terpenoids from tropical green algae of the family Udoteaceae. Eleventh International Seaweed Symposium: 135–140. https://doi.org/10.1007/978-94-009-6560-7_20
Flora do Brasil (2020) Jardim Botânico of Rio de Janeiro. Available from: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB99286 (accessed 17 July 2022)
Freshwater, D.W., Fredericq, S., Butler, S.B., Hommersand, M.H. & Chase, M.W. (1994) A gene phylogeny of the red algae (Rhodophyta) based on rbcL. Proceedings of National Academy of Sciences of the United States of America 91: 7281–7285. https://doi.org/10.1073/pnas.91.15.7281
Folmer, F., Jaspars, M., Dicato, M. & Diederich, M. (2010) Photosynthetic marine organisms as a source of anticancer compounds. Phytochemistry Reviews 9: 557–579. https://doi.org/10.1007/s11101-010-9200-2
Freshwater, D.W. & Rueness, J. (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33: 187–194. https://doi.org/10.2216/i0031-8884-33-3-187.1
Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62: 707–724. https://doi.org/10.1093/sysbio/syt033
Guimarães, N.C.L., Reis, T.N.V. & Cocentino, A.L.M. (2008) Chlorophyta bentônicas da zona econômica exclusiva do Nordeste brasileiro (REVIZEE NE-I). Insula 37: 35–52.
Guiry, M.D. & Guiry, G.M.E. (2022) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. (accessed 15 July 2022).
Gepp, A. & Gepp, E.S. (1911) The Codiaceae of the Siboga Expedition including a monograph of Flabellarieae and Udoteae Siboga-ExpeditieMonographie LXII. Leiden: E. J. Brill, pp. 1–150. 
Häendeler, K., Wägele, H., Wahrmund, U., Rüdinger, M. & Knoop, V. (2010) Slugs’ last meals: molecular identification of sequestered chloroplasts from different algal origins in Sacoglossa (Opisthobranchia, Gastropoda). Molecular Ecology Resources 10: 968–978. https://doi.org/10.1111/j.1755-0998.2010.02853.x
Howe, M.A. (1904) Notes on Bahaman algae. Bulletin of the Torrey Botanical Club 31: 91–100. https://doi.org/10.2307/2478494
Howe, M.A. (1928) Notes on some marine algae from Brazil and Barbados. Journal of the Washington Academy of Sciences 18: 186–194.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S. & Duran, C. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kooistra, W. (2002) Molecular phylogenies of Udoteaceae (Bryopsidales, Chlorophyta) reveal non monophyly for Udotea, Penicillus and Chlorodesmis. Phycologia 41: 453–462. https://doi.org/10.2216/i0031-8884-41-5-453.1
Kützing, F.T. (1843) Phycologia general isoder Anatomie, Physiologie und Systemkunde der Tange. Leipzig: Brockhaus, F. A. https://doi.org/10.5962/bhl.title.4746
Lagourgue, L., Puillandre, N. & Payri, C.E. (2018) Exploring the Udoteaceae diversity (Bryopsidales, Chlorophyta) in the Caribbean region based on molecular and morphological data. Molecular Phylogenetics and Evolution 127: 758–769. https://doi.org/10.1016/j.ympev.2018.06.023
Lagourgue, L. & Payri, C.E. (2020) Large-scale diversity reassessment, evolutionary history, and taxonomic revision of the green macroalgae family Udoteaceae (Bryopsidales, Chlorophyta). Journal of Systematics and Evolution 60: 101–127. https://doi.org/10.1111/jse.12716
Lam, D.W. & Zechman, F.W. (2006) Phylogenetic analyses of the Bryopsidales (Ulvophyceae, Chlorophyta) based on Rubisco large subunit gene sequences. Journal of Phycology 42: 669–678. https://doi.org/10.1111/j.1529-8817.2006.00230.x
Lamarck, J.B.P.A. (1813) Sur les polypiers empâtés. Annales du Muséum d’Histoire Naturelle 20: 294–312, 370–386, 432–458.
Lamouroux, J.V.F. (1812) Extrait d’un mémoire sur la classification des Polypiers coralligènes non entièrement pierreux. Nouveaux Bulletin des Sciences, par la Société Philomathique de Paris 3: 181–188.
Littler, D.S. & Littler, M. (1990) Systematics of Udotea species (Bryopsidales, Chlorophyta) in the tropical western Atlantic. Phycologia 29: 206–252. https://doi.org/10.2216/i0031-8884-29-2-206.1
Littler, D.S. & Littler, M. (2000) Caribbean Reef Plants. OffShore Graphics, Washington, pp. 422–434.
Montagne, J.F.C. (1842) Prodromus generum specierumque phycearum novarum, in itinere ad polum antarcticum...ab illustri Dumont d’Urville peracto collectarum, notis diagnosticis tantum huc evulgatarum, descriptionibus verò fusioribus nec non iconibus analyticis iam iamque illustrandarum. Paris: apud Gide, editorem. pp. 1–16.
Minh, B.Q., Nguyen, M.A.T. & von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30: 1188–1195. https://doi.org/10.1093/molbev/mst024
Nakatsu, T., Ravi, B.N. & Faulkner, D.J. (1981) Antimicrobial constituents of Udotea flabellum. The Journal of Organic Chemistry 46 (12): 2435–2438. https://doi.org/10.1021/jo00325a001
Nguyen, L.T., Schmidt, H.A., Haeseler, A.V. & Minh, B. (2015) Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
Oliveira-Carvalho, M.F., Pereira, S.M.B. & Zickel, C.S. (2003) Florística e distribuição espaço-temporal das clorofíceas bentônicas em trechos recifais do litoral norte do estado de Pernambuco, Brasil. Hoehnea 30: 201–202.
Oliveira, M.G.T., Pereira, S.M.B., Benko-Isepon, A.M., Balbino, V.Q., Silva Júnior, W.J., Oliveira Carvalho, M.F.O. & Cassano, V. (2020) First molecular analysis of the genus Bryopsis (Bryopsidales, Chlorophyta) from Brazil, with an emphasis on the Pernambuco coast. Acta Botanica Brasilica 35: 161 –178. https://doi.org/10.1590/0102-33062020abb0154
Pereira, S.M.B. (1974) Clorofíceas marinhas da Ilha de Itamaracá e Arredores. Universidade de São Paulo, São Paulo. 184 pp. 
Pereira, S.M.B. & Accioly, M.C. (1998) Clorofíceas Bentônicas da Praia de Serrambi, Pernambuco, Brasil. Acta Botanica Brasilica 12: 25–52. https://doi.org/10.1590/S0102-33061998000100003
Pereira, S.M.B., Oliveira-Carvalho, M.F., Angeiras, J.A.P., Pedrosa-Pedrosa, M.E., Oliveira, N.M.B., Torres, J. Gestinari, L.M.S., Cocentino, A.L.M, Santos, M.D., Nascimento, P.R. & Cavalcanti, D.R. (2002) Algas marinhas bentônicas do Estado de Pernambuco. v. 1. Recife, Diagnostico da Biodiversidade de Pernambuco, pp. 97–124.
Pereira, S.M.B., Ribeiro, F.A. & Bandeira-Pedrosa, M.E. (2007) Algas pluricelulares do infralitoral da praia de Gaibú (Pernambuco-Brasil). Revista Brasileira de Biociências 5: 951–953. 
Pereira, S.M.B., Moura, C.W.N., Gestinari, L.M.S., Bandeira-Pedrosa, M.E., Alves, A.M., Santos, A.A., Alves, G.L., Oliveira, I.S., Oliveira, I.B., Moniz-Brito, K.L., Oliveira-Carvalho, M.F., Andrade, N.A., Freitas, N.S. & Brayner-Barros, S. (2011) Taxonomia das clorofitas marinhas. In: Pedrini, A.G. (Org.) (2011) Macroalgas (Chlorophyta) e gramas (Magnoliophyta) marinhas do Brasil. Techinical Books, Rio de Janeiro, pp. 41–99.
Pereira, S.M.B., Torres, J. & Gestinari, L.M.S. (2014) Composition and Distribution of Deep Water Macroalgae Species from the Continental Shelf of Sergipe State, Brazil. Phytotaxa 190: 250–267. https://doi.org/10.11646/phytotaxa.190.1.15
Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609. https://doi.org/10.1080/10635150600852011
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21: 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
Puillandre, N., Brouillet, S. & Achaz, G. (2020) ASAP: Assemble Species by Automatic Partitioning. Molecular Ecology Resources 21: 609–620. https://doi.org/10.1111/1755-0998.13281
Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, C.-H., Xie, D., Zhang, C., Stadler, T. & Drummond, A.J. (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15: e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Ries, J.B. (2009) Aragonite production in calcite seas: effect of seawater Mg/Ca ratio on the calcification and growth of the calcareous alga Penicillus capitatus. Paleobiology 31: 445–458. https://doi.org/10.1666/0094-8373(2005)031[0445:APICSE]2.0.CO;2
Rocha, M.C.B.S. (2016) Taxonomia e distribuição do gênero Udotea J V Lamour. (Bryopsidales, Chlorophyta) no litoral brasileiro. Universidade Federal Rural de Pernambuco, Recife. 76 pp.
Santos, G.N. & Nunes, J.M.C. (2014) Udoteaceae (Bryopsidales, chlorophyta) no litoral do estado da Bahia, Brasil. Sitientibus série Ciências Biológicas 436: 14–21. https://doi.org/10.13102/scb436
Saunders, G.W. & Kucera, H. (2010) An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogamie, Algologie 31: 487–528.
Sauvage, T., Ballantine, D.L., Peyton, K.A., Wade, R.M., Sherwood, A.R., Keeley, S. & Smith, C. (2020) Molecular confirmation and morphological reassessment of Udotea geppiorum (Bryopsidales, Chlorophyta) with ecological observations of mesophotic meadows in the Main Hawaiian Islands. European Journal of Phycology 55: 186–196. https://doi.org/10.1080/09670262.2019.1668061
Sissini, M., Oliveira, M.C., Horta, P.A. & Pellizzari, F.M. (2017) Macroalgas da Ilha da Trindade. In: Secretaria da Comissão Interministerial para os Recursos do Mar - SECIRM. (Org.) PROTRINDADE: programa de pesquisas científicas na Ilha de Trindade. 10 anos de pesquisas (SECIRM). Vol. 1. SECIRM, Brasília, pp. 99–108.
Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (and other methods), version, 4, b10. Sunderland, MA, USA, Sinauer Associates.
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.
Torrano-Silva, B.N. & Oliveira, E.C. (2013) Macrophytobenthic flora of the Abrolhos Archipelago and the Sebastião Gomes Reef, Brazil. Continental Shelf Research 70: 150–158. https://doi.org/10.1016/j.csr.2013.09.019
Verbruggen,H., Ashworth, M., LoDuca, S.T., Vlaeminck, C., Cocquyt, E., Sauvage, T., Zechman, F.W., Littler, D.S., Littler, M.M., Leliaert, F. & De Clerck, O. (2009) A multilocus time-calibrated phylogeny of the siphonous green algae. Molecular Phylogenetics and Evolution 50: 642–653. https://doi.org/10.1016/j.ympev.2008.12.018
Villaça, R., Pedrini, A.G., Pereira, S.M.B. & Figueiredo, M.D.O. (2006) Flora marinha bentônica das ilhas oceânicas brasileiras. In: Ilhas Oceânicas Brasileiras da Pesquisa ao Manejo. Ministério do Meio Ambiente, Brasília, pp. 105–146.
Wynne, M.J. (2017) A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145: 1–202.
Ximenes, C.F., Cassano, V., Oliveira-Carvalho, M.F., Gurgel, C.F.D., Verbruggen, H. & Pereira, S.M.B. (2017) Systematics of the genus Halimeda (Bryopsidales, Chlorophyta) in Brazil including the description of Halimeda jolyana sp.nov. Phycologia 56: 369–381. https://doi.org/10.2216/16-77.1
Yoneshigue-Valentin, Y, Gestinari, L.M.S. & Fernandes, D.R.P. (2006) Macroalgas da Plataforma Continental de Salvador (estado da Bahia) ao Cabo de São Tomé (norte do estado do Rio de Janeiro), Brasil. In: Lavrado, H.P. & Ignacio, B.L. (Eds.) Biodiversidade bentônica da região central da Zona Econômica Exclusiva brasileira. Museu Nacional (Série Livros n. 18), Rio de Janeiro, pp. 67–105.
Zhang, J., Kapli, R., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, Advance Access 29: 2869–2876. https://doi.org/10.1093/bioinformatics/btt499