Abstract
We used three molecular markers (COI-5P, rbcL and UPA) to investigate the diversity of Hypnea spp., an economically important red algal genus, collected from India. Our concatenated tree (COI-5P and rbcL) supported the monophyly of two new species, Hypnea indica sp. nov. and Hypnea bullata sp. nov. H. indica diverged from its closest two sister species, Hypnea cervicornis and Hypnea tenuis (by 15.9 and 11.2%, respectively, in COI-5P; and 3.4 and 3.2% in rbcL). We describe H. indica as a new species characterised by an erect, percurrent main axis with spine-like branchlets in acute angles, straight and forked apices, axial cells surrounded by large periaxial cells or two cells similar in size to the axial cell, and the presence of lenticular thickening in the cross-section of the thallus. H. bullata diverged from its closest sister species, Hypnea brasiliensis (by 10.9% in COI-5P and 3.3% in rbcL). H. bullata is characterized by a prostrate thallus up to 1.5 cm in height, highly anastomosed, with an axial cell surrounded by similar sized, or smaller, periaxial cells, tetrasporangia present near the base of branchlets, and the presence of lenticular thickening.
Funding source: DST-SERB Core Research Grant
Award Identifier / Grant number: CRG/20l9/005499
About the authors
Pushpendu Kundu is a PhD candidate of the Centre for Biosciences, Central University of Punjab, India. His major field of research includes the taxonomy, phylogeography, evolution and biogeography of marine macroalgae. His current research focuses on biodiversity characterization of Florideophyceae from the Indian coast and the eastern Antarctica coast based upon molecular taxonomy-assisted polyphasic approach.
Dr Felix Bast is an associate professor and science writer based at the Central University of Punjab, Bathinda, Punjab, India where he is heading the Department of Botany. He earned his PhD degree in marine biology from MEXT, Japan. He has research interest in marine biology, taxonomy, phylogeography, molecular systematics of algae and liberal arts. He is a known science communicator in India through his writings, outreach talks and YouTube videos fostering critical thinking and scientific skepticism.
Acknowledgments
We are thankful to three anonymous reviewers for their constructive criticisms that have substantially helped to improve a previous version of this manuscript.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: This study was supported by a grant from the Department of Science and Technology-Government of India, SERB Core Research Grant, awarded to F.B. (Grant No. CRG/20l9/005499). P.K. thanks the Central University of Punjab for the financial support for his PhD research work.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Agardh, J.G. (1851). Species genera et ordines algarum, seu descriptiones succinctae specierum, generum et ordinum, quibus algarum regnum constituitur. Volumen secundum: algas florideas complectens. Sweden: C.W.K. Gleerup.Search in Google Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403–410, https://doi.org/10.1016/s0022-2836(05)80360-2.Search in Google Scholar
Arman, M. and Qader, S.A.U. (2012). Structural analysis of kappa-Carrageenan isolated from Hypnea musciformis (red algae) and evaluation as an elicitor of plant defense mechanism. Carbohydr. Polym. 88: 1264–1271, https://doi.org/10.1016/j.carbpol.2012.02.003.Search in Google Scholar
Bast, F., Bhushan, S., and John, A.A. (2014). Morphological and molecular assessment of native carrageenophyte Hypnea valentiae (Cystocloniaceae, Gigartinales) in Indian Subcontinent. Phykos 44: 52–58.Search in Google Scholar
Børgesen, F. (1934). Some Indian rhodophyceae especially from the shores of the presidency of Bombay: IV. Bull. Misc. Inform. Kew IV: 1–30.10.2307/4111648Search in Google Scholar
Clarkston, B.E. and Saunders, G.W. (2010). A comparison of two DNA barcode markers for species discrimination in the red algal family Kallymeniaceae (Gigartinales, Florideophyceae), with a description of Euthora timburtonii sp. nov. Botany 88: 119–131, https://doi.org/10.1139/b09-101.Search in Google Scholar
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772, https://doi.org/10.1038/nmeth.2109.Search in Google Scholar
de Jesus, P.B., Nauer, F., Lyra, G.M., Cassano, V., Oliveira, M.C., Nunes, J.M.C., and Schnadelbach, A.S. (2016). Species‐delimitation and phylogenetic analyses of some cosmopolitan species of Hypnea (Rhodophyta) reveal synonyms and misapplied names to H. cervicornis, including a new species from Brazil. J. Phycol. 52: 774–792, https://doi.org/10.1111/jpy.12436.Search in Google Scholar
Drummond, A.A., Cheung, B., Heled, M., Kearse, J., Moir, M., Stones-Havas, R., Thierer, S., and Wilson, A.T. (2010). Geneious v 8.0. 5. Biomatters. Available at: http://www.geneious.com.Search in Google Scholar
Fredericq, S., Hommersand, M.H., and Freshwater, D.W. (1996). The molecular systematics of some agar-and carrageenan-containing marine red algae based on rbcL sequence analysis. Hydrobiologia 326/327: 125–135, https://doi.org/10.1007/bf00047797.Search in Google Scholar
Freshwater, D.W. and 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.Search in Google Scholar
Geraldino, P.J.L., Riosmena‐Rodriguez, R., Liao, L.M., Boo, and Min, S. (2010). Phylogenetic relationships within the genus Hypnea (Gigartinales, Rhodophyta), with a description of H. caespitosa sp. nov. J. Phycol. 46: 336–345, https://doi.org/10.1111/j.1529-8817.2009.00804.x.Search in Google Scholar
Geraldino, P.J.L., Yang, E.C., Sook Kim, M., and Min Boo, S. (2009). Systematics of Hypnea asiatica sp. nov.(Hypneaceae, Rhodophyta) based on morphology and nrDNA SSU, plastid rbcL, and mitochondrial cox1. Taxon 58: 606–616, https://doi.org/10.1002/tax.582023.Search in Google Scholar
Greer, C.W., Shomer, I., Goldstein, M.E., and Yaphe, W. (1984). Analysis of carrageenan from Hypnea musciformis by using κ-and ι-carrageenanases and 13C-NMR spectroscopy. Carbohydr. Res. 129: 189–196, https://doi.org/10.1016/0008-6215(84)85311-2.Search in Google Scholar
Guiry, M.D. and Guiry, G.M. (2020). AlgaeBase. Galway: World-wide electronic publication. National University of Ireland, Available at: https://www.algaebase.org/ (Accessed 5 November 2020).Search in Google Scholar
Hayee-Memon, A. and Shameel, M. (1996). A taxonomic study of some red algae commonly growing on the coast of Karachi. PJMS 5: 113–136.Search in Google Scholar
Isaac, W. and Hewitt, F. (1953). The morphology, geographical distribution and ecology of Hypnea spicifera (Suhr) Harv. J. S. Afr. Bot. 19: 73–84.Search in Google Scholar
Jesus, P.B., Nauer, F., Lyra, G.M., Cassano, V., Oliveira, M.C., Nunes, J.M.C., and Schnadelbach, A.S. (2016). Species delimitation and phylogenetic analyses of some cosmopolitan species of Hypnea (Rhodophyta) reveal synonyms and misapplied names to H. cervicornis, including a new species from Brazil. J. Phycol. 52: 1–44.10.1111/jpy.12436Search in Google Scholar
Johnson, V.J. (2018). Molecular systematics of the genus Hypnea (Rhodophyta) in South Africa, with the description of a new genus, Tenebris (Cystocloniaceae, Rhodophyta), PhD thesis. Cape Town, South Africa: University of Cape Town.Search in Google Scholar
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547–1549, https://doi.org/10.1093/molbev/msy096.Search in Google Scholar
Lamouroux, J.V. (1813). Essay on the genera of the family of nonarticulated thalassiophytes. Paris: Belin’s Printing Press.Search in Google Scholar
Leliaert, F., Verbruggen, H., Vanormelingen, P., Steen, F., López-Bautista, J.M., Zuccarello, G.C., and De Clerck, O. (2014). DNA-based species delimitation in algae. Eur. J. Phycol. 49: 179–196, https://doi.org/10.1080/09670262.2014.904524.Search in Google Scholar
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452, https://doi.org/10.1093/bioinformatics/btp187.Search in Google Scholar
Masuda, M., Yamagishi, Y., Chiang, Y.M., Lewmanomont, K., and Xia, B.M. (1997). Overview of Hypnea (Rhodophyta, Hypneaceae). In: Abbott, I.A. (Ed.), Taxonomy of economic seaweeds, California Sea Grant College. La Jolla, California: University of California, pp. 127–133.Search in Google Scholar
Nauer, F., Guimarães, N.R., Cassano, V., Yokoya, N.S., and Oliveira, M.C. (2014). Hypnea species (Gigartinales, Rhodophyta) from the southeastern coast of Brazil based on molecular studies complemented with morphological analyses, including descriptions of Hypnea edeniana sp. nov. and H. flava sp. nov. Eur. J. Phycol. 49: 550–575, https://doi.org/10.1080/09670262.2014.981589.Search in Google Scholar
Nauer, F., Cassano, V., and Oliveira, M.C. (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, https://doi.org/10.1007/s10811-014-0488-y.Search in Google Scholar
Nauer, F., Jesus, P.B., Cassano, V., Nunes, J.M.C., Schnadelbach, A.S., and Oliveira, M.C. (2019). A taxonomic review of the genus Hypnea (Gigartinales, Rhodophyta) in Brazil based on DNA barcode and morphology. Rev. Bras. Bot. 42: 561–574, https://doi.org/10.1007/s40415-019-00544-z.Search in Google Scholar
Papenfuss, G.F. (1958). Notes on algal nomenclature. IV. Various genera and species of Chlorophyceae, Phaeophyceae and Rhodophyceae. Taxon 7: 104–109, https://doi.org/10.2307/1217432.Search in Google Scholar
Rambaut, A., Suchard, M., and Drummond, A. (2009). Tracer ver. 1.5, Available at: tree.bio.ed.ac.uk/software/tracer.Search in Google Scholar
Ronquist, F. and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574, https://doi.org/10.1093/bioinformatics/btg180.Search in Google Scholar
Saunders, G.W. (2005). Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Proc. Roy. Soc. Lond. B 360: 1879–1888, https://doi.org/10.1098/rstb.2005.1719.Search in Google Scholar
Saunders, G.W. and Moore, T.E. (2013). Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28: 31–43, https://doi.org/10.4490/algae.2013.28.1.031.Search in Google Scholar
Sherwood, A.R. and Presting, G.G. (2007). Universal primers amplify a 23S rDNA plastid marker in eukaryotic algae and cyanobacteria 1. J. Phycol. 43: 605–608, https://doi.org/10.1111/j.1529-8817.2007.00341.x.Search in Google Scholar
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313, https://doi.org/10.1093/bioinformatics/btu033.Search in Google Scholar
Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57: 758–771, https://doi.org/10.1080/10635150802429642.Search in Google Scholar
Stöver, B.C. and Müller, K.F. (2010). TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinf. 11: 7, https://doi.org/10.1186/1471-2105-11-7.Search in Google Scholar
Tanaka, T. (1941). The genus Hypnea from Japan. Japan. Sc. Papers Inst. Alg. Res. Hokkaido Univ. 2: 227–250.Search in Google Scholar
Turner, D. (1809). Fuci sive plantarum fucorum generi a botanicis ascriptarum icones descriptiones et historia, Vol. II. London: J. M’Creery.Search in Google Scholar
Vasey, D.E., Fredericks, S.E., Shen, L., and Thompson, S. (2011). Natural resources and sustainability. United States: Berkshire Publishing Group.Search in Google Scholar
Weber-van Bosse, A. (1913). IV. Marine Algæ, rhodophyceæ, of the ‘Sealark’ Expedition, collected by Mr. J. Stanley Gardiner, MA. Trans. Linn. Soc. Lond. 2nd Series. Botany 8: 105–142, https://doi.org/10.1111/j.1095-8339.1913.tb00282.x.Search in Google Scholar
Yokoya, N.S., Nauer, F., and Oliveira, M.C. (2020). Concise review of the genus Hypnea JV Lamouroux, 1813. J. Appl. Phycol. 32: 3585–3603, https://doi.org/10.1007/s10811-020-02209-x.Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2020-0069).
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