Molecular and morphological reappraisal of Spyridiocolax capixabus (Spyridiaceae, Rhodophyta), a rare endemic parasite from Brazil

  • 1 Postgraduate Program “Biodiversidade Vegetal e Meio Ambiente”, Instituto de Botânica, Av. Miguel Estéfano, 3687, São Paulo 04301-012, Brazil
  • 2 Núcleo de Pesquisa em Ficologia, Instituto de Botânica, São Paulo 04301-012, Brazil
Daniella Harumi Chen
  • Postgraduate Program “Biodiversidade Vegetal e Meio Ambiente”, Instituto de Botânica, Av. Miguel Estéfano, 3687, São Paulo 04301-012, Brazil
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  • Daniella Harumi Chen graduated in Biological Sciences at the Universidade Presbiteriana Mackenzie. She has worked as a technician at the Laboratory of Marine Phycology, Institute of Botany, São Paulo. She has experience in the area of Molecular Biology with emphasis on taxonomy and DNA barcoding of marine macroalgae. She received her Master’s degree in Plant Biodiversity and Environment with studies on the holotypes of Ceramiales (Rhodophyta) from Brazil housed at SP and SPF herbaria.
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, Luanda Pereira SoaresORCID iD: https://orcid.org/0000-0002-4207-5022
  • Núcleo de Pesquisa em Ficologia, Instituto de Botânica, São Paulo 04301-012, Brazil
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  • Luanda Pereira Soares is a postdoctoral researcher at the Nucleus for Research in Phycology, Institute of Botany, São Paulo, Brazil. She received her PhD in Plant Biodiversity and Environment in 2015 at the same institution, and since then, she has been developing studies related to floristic surveys of Rhodophyta, using classical taxonomy and molecular tools. At present, her research includes taxonomy and molecular phylogeny of marine macroalgae, focusing on reassessment of type specimens, endemic and rare marine algae occurring along the Brazilian coast.
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and Mutue Toyota FujiiORCID iD: https://orcid.org/0000-0001-6752-1570
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  • Núcleo de Pesquisa em Ficologia, Instituto de Botânica, São Paulo 04301-012, Brazil
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  • Mutue Toyota Fujii is a Scientific Researcher at the Nucleus for Research in Phycology, Institute of Botany, São Paulo, Brazil. She received her Master and PhD degrees in Plant Biology from the São Paulo State University for her studies on morphological, chemical and cytogenetical approaches on Laurencia s.l. (Rhodophyta) from Brazil. Currently, she is a coordinator of the Postgraduate Program in Plant Biodiversity and Environment (PPG-IBt) and her area of activity is taxonomy, phylogeny, phylogeography and biogeography of marine macroalgae.
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Abstract

The monotypic red algal parasite genus Spyridiocolax was proposed from material from the coast of Espírito Santo to accommodate Spyridiocolax capixabus, endemic from Brazil. The species is rare, and we performed a morphological reappraisal and the first molecular characterization of S. capixabus. Parasite specimens growing on Spyridia clavata were collected in the type locality, Itaoca Beach, Espírito Santo. Spyridiocolax capixabus forms colorless warts on the branches of S. clavata, and the secondary pit connections were described for the first time. Male, female and tetrasporophytic structures were observed growing in the same host plant. The plastid rbcL sequences of parasite and host were identical. A divergence of one nucleotide was found to the nuclear SSU rRNA gene, suggesting that the parasite retains the chloroplast of its host. Both plastidial and nuclear phylogenies supported the close relationship of S. capixabus and S. clavata. The data obtained corroborate other studies with rhodophycean parasites, which show morphological and molecular similarities between parasites and hosts. To maintain the monophyly of the host genus, the transfer of S. capixabus to Spyridia is proposed here on the basis of morphological and molecular evidence. Our study constitutes a starting point for reinvestigating the red algal parasites in Brazil.

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  • Apt, K.E. and K.E. Schlech. 1998. Ululania stellata gen. et sp. nov. (Rhodomelaceae), a new genus and species of parasitic red algae from Hawaii. Phycologia 37: 157–161.

    • Crossref
    • Export Citation
  • Batters, E.A.L. 1892. Gonimophyllum buffhami: a new marine algae. J. Bot. 30: 65–67.

  • Benson, D.A., M. Cavanaugh, K. Clark, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell and E.W. Sayers. 2013. GenBank. Nucleic Acids Res. 41: 36–42.

  • Blouin, N.A. and C.E. Lane. 2012. Red algal parasites: Models for a life history evolution that leaves photosynthesis behind again and again. Bioessays 34: 226–235.

    • Crossref
    • PubMed
    • Export Citation
  • de Queiroz, K. 2012. Biological nomenclature from Linnaeus to the PhyloCode. Bibli. Herpetol. 9: 135–145.

  • de Queiroz, K. and J. Gauthier. 1992. Phylogenetic taxonomy. Annu. Rev. Ecol. Syst. 23: 449–480.

    • Crossref
    • Export Citation
  • de Queiroz, K. and J. Gauthier. 1994. Toward a phylogenetics system of biological nomenclature. Trends Ecol. Evol. 9: 27–31.

    • Crossref
    • Export Citation
  • Feldmann, J. and G. Feldmann. 1958. Recherches sur quelques Floridées parasites. Rev. Gen. Bot. 65: 49–128.

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    • Crossref
    • PubMed
    • Export Citation
  • Freese, J.L. and C.E. Lane. 2017. Parasitism finds many solutions to the same problems in red algae (Florideophyceae, Rhodophyta). Mol. Biochem. Parasitol. 24: 105–111.

  • Freshwater, D.W. and J. Rueness. 1994. Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33: 187–194.

    • Crossref
    • Export Citation
  • Fujii, M.T. and S.M.P.B. Guimarães. 1999. Morphological studies of the parasitic red alga Janczewskia moriformis (Rhodomelaceae, Ceramiales) from Brazil. Phycologia 38: 1–7.

    • Crossref
    • Export Citation
  • Goff, L.J. 1982. The biology of parasitic red algae. In: (F.E. Round and D.J. Chapman, eds) Progress in Phycological Research. Elsevier Biomedical Press, Amsterdam. pp. 289–369.

  • Goff, L.J. and A.W. Coleman. 1995. Fate of parasite and host organelle DNA during cellular-transformation of red algae by their parasites. Plant Cell 7: 1899–1911.

    • Crossref
    • PubMed
    • Export Citation
  • Goff, L.J., D.A. Moon, P. Nyvall, B. Stache, K. Mangin and G.C. Zuccarello. 1996. The evolution of parasitism in the red algae: molecular comparisons of aldephoparasites and their hosts. J. Phycol. 32: 297–312.

    • Crossref
    • Export Citation
  • Goff, L.J., J. Ashen and D. Moon. 1997. The evolution of parasites from their hosts: a case study in the parasitic red algae. Evolution 51: 1068–1078.

    • Crossref
    • PubMed
    • Export Citation
  • Guimarães, S.M.P.B. 1993. Morphology and systematics of the red algal parasite Dawsoniocolax bostrychiae (Choreocolacaceae, Rhodophyta). Phycologia 32: 251–258.

    • Crossref
    • Export Citation
  • Guindon, S., J.-F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk and O. Gascuel. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59: 307–321.

    • Crossref
    • PubMed
    • Export Citation
  • Guiry, M.D. and G.M. Guiry. 2019. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org.

  • Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.

  • Hörandl, E. 2006. Paraphyletic versus monophyletic taxa–evolutionary versus cladistic classifications. Taxon 55: 564–570.

    • Crossref
    • Export Citation
  • Joly, A.B. 1966. Centrocerocolax, a new parasitic genus of Rhodophyta. Rickia 2: 73–77.

  • Joly, A.B. and E.C. Oliveira Filho. 1966. Spyridiocolax and Heterodasya two new genera of the Rhodophyceae. Sellowia 18: 115–125.

  • Joly, A.B. and N. Yamaguishi-Tomita. 1967. Dawsoniella bostrychiae: a new parasite of mangrove algae. Sellowia 19: 63–70.

  • Kim, M.-S. and G.-Y. Cho. 2010. A new red algal parasite, Symphyocolax koreana gen. et. sp. nov. (Rhodomelaceae, Ceramiales), from Korea. Algae 25: 105–113.

    • Crossref
    • Export Citation
  • Kraft, G.T. and I.A. Abbott. 2002. The anatomy of Neotenophycus ichthyosteus gen. et sp. nov. (Rhodomelaceae, Ceramiales), a bizarre red algal parasite from the central Pacific. Eur. J. Phycol. 37: 269–278.

    • Crossref
    • Export Citation
  • Kurihara, A., T. Abe, M. Tani and A.R. Sherwood. 2010. Molecular phylogeny and evolution of red algal parasites: a case study of Benzaitenia, Janczewskia, and Ululania (Ceramiales). J. Phycol. 46: 580–590.

    • Crossref
    • Export Citation
  • Lin, S.M., S. Fredericq and M.H. Hommersand. 2001. Systematics of the Delesseriaceae (Ceramiales, Rhodophyta) based on large subunit rDNA and rbcL sequences, including the Phycodryoideae subfam. nov. J. Phycol. 37: 881–899.

    • Crossref
    • Export Citation
  • Milne, I., D. Lindner, M. Bayer, D. Husmeier, G. McGuire, D.F. Marshall and F. Wright. 2009. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25: 126–127.

    • Crossref
    • PubMed
    • Export Citation
  • Ng, P.-K., P.-E. Lim and S.-M. Phang. 2014a. Radiation of the red algal parasite Congracilaria babae onto a secondary host species, Hydropuntia sp. (Gracilariaceae, Rhodophyta). PLoS One 9: e0097450.

  • Ng, P.-K., P.-E. Lim, A. Kato and S.-M. Phang. 2014b. Molecular evidence confirms the parasite Congracilaria babae (Gracilariaceae, Rhodophyta) from Malaysia. J. Appl. Phycol. 26: 1287–1300.

    • Crossref
    • Export Citation
  • Oliveira Filho, E.C. 1969. Algas marinhas do sul do estado do Espírito Santo (Brasil). I – Ceramiales. Bol. Fac. Filos. Cienc. Let. Univ. São Paulo (Botânica 26) 343: 1–277.

  • Oliveira Filho, E.C. and Y. Ugadim. 1973. Levringiella polysiphoniae a new species of parasitic red algae (Rhodophyta-Rhodomelaceae) from Brazil. Bol. Bot. Univ. São Paulo 1: 95–99.

  • Posada, D. and K.A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817–818.

    • Crossref
    • PubMed
    • Export Citation
  • Preuss, M. and G.C. Zuccarello. 2014. What’s in a name? Monophyly of genera in the red algae: Rhodophyllis parasitic sp. nov. (Gigartinales, Rhodophyta): a new red algal parasite from New Zealand. Algae 29: 279–288.

    • Crossref
    • Export Citation
  • Preuss, M. and G.C. Zuccarello. 2018. Three new red algal parasites from New Zealand: Cladhymenia oblongifoliaphila sp. nov. (Rhodomelaceae), Phycodrys novae-zelandiaephila sp. nov. (Delesseriaceae) and Judithia parasitica sp. nov. (Kallymeniaceae). Phycologia 57: 9–19.

    • Crossref
    • Export Citation
  • Preuss, M., W.A. Nelson and G.C. Zuccarello. 2017. Red algal parasites: a synopsis of described species, their hosts, distinguishing characters and areas for continued research. Bot. Mar. 60: 13–25.

  • Reinsch, P.F. 1875. Contributiones ad algologiam et fungologiam. Vol. I. T.O. Welgel, Lipsiae. pp. 422.

  • Ronquist, F., M. Teslenko, P. Van der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard and J.P. Huelsenbeck. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.

    • Crossref
    • PubMed
    • Export Citation
  • Saunders, G.W. and G.T. Kraft. 1994. Small-subunit rRNA gene sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). 1. Evidence for the Plocamiales ord. nov. Can. J. Bot. 72: 1250–1263.

    • Crossref
    • Export Citation
  • Setchell, W.A. 1918. Parasitism among the red algae. Proc. Am. Philos. Soc. 57: 155–172.

  • Thiers, B. 2019. Index Herbariorum. A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/.

  • Vergés, A., C. Izquierdo and M. Verlaque. 2005. Rhodymeniocolax mediterraneus sp. nov. (Rhodymeniales, Rhodophyta), parasitic on Rhodymenia ardissonei from the western Mediterranean Sea. Phycologia 44: 510–516.

    • Crossref
    • Export Citation
  • West, J.A. and H.P. Calumpong. 1988. Dawsoniocolax bostrychiae (Choreocolacaceae, Gigartinales), an alloparasitic red alga new to Australia. Phycologia 27: 463–468.

    • Crossref
    • Export Citation
  • Wynne, M.J. and F. Scott. 1989. Pitycolax, a new genus of adelphoparasitic red algae from lle Amsterdam, Southern Indian Ocean. Cryptogam. Algol. 10: 23–32.

  • Yoneshigue, Y. 1985. Taxonomie et ecologie des algues marines dans la region de Cabo Frio (Rio de Janeiro, Brasil). Unpublished doctoral thesis, L’Universite D’Aix-Marseille II, Merseille, France. pp. 466.

  • Yoneshigue, Y. and E.C. Oliveira Filho. 1984. Algae from Cabo Frio upwelling area. 2. Gelidiocolax pustulata (Gelidiaceae, Rhodophyta): an unusual new putative parasitic species. J. Phycol. 20: 440–443.

    • Crossref
    • Export Citation
  • Zuccarello, G.C. and J.A. West. 1994. Host specificity on the red algal parasites Bostrychiocolax australis gen. et sp. nov. and Dawsoniocolax bostrychiae (Choreocolacaceae, Rhodophyta). J. Phycol. 30: 137–146.

    • Crossref
    • Export Citation
  • Zuccarello, G.C., D. Moon and L.J. Goff. 2004. A phylogenetic study of parasitic genera placed in the family Choreocolacaceae (Rhodophyta). J. Phycol. 40: 937–945.

    • Crossref
    • Export Citation
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