Abstract
Kumanoa belonging to the order Batrachospermales is the most species-rich and widely distributed genus of freshwater red algae in China. In this study, a new Kumanoa species is described and illustrated from Baiyun Mountain, Guangdong, China, based on morphological observations and phylogenetic analysis. Kumanoa baiyunensis sp. nov is morphologically distinguished from other species by presenting a small habit (0.5–1 cm tall) with abundant branching in upper part of the thallus; carposporophytes spherical and one per whorl; club-shaped trichogynes with distinct stalk; spermatangia sparse and single-grown, terminal on primary fascicles. Phylogenetic analysis based on the concatenated rbcL+COI-5P+UPA alignment places Kumanoa baiyunensis in a well-supported clade (98/0.96, bootstrap proportion/posterior probability) sister to K. faroensis (from USA) and K. spermatiophora (from Hawaii) with high divergence (rbcL: 4.9%–5.0%, COI-5P: 10.1%–10.5%, UPA: 2.3%). In addition, K. baiyunensis can be easily distinguished from ten Kumanoa species reported in China through morphological features such as small thallus size, abundant branching in upper parts of the thallus, and spermatangia sparse, single-grown, and terminal on primary fascicles. The description of this new species expands the diversity of genus Kumanoa in the world.
References
Entwisle, T.J., Vis, M.L., Chiasson, W.B., Necchi, O.Jr. & Sherwood, A.R. (2009) Systematics of the Batrachospermales (Rhodophyta)–a synthesis. Journal of Phycology 45 (3): 704–715. https://doi.org/10.1111/j.1529-8817.2009.00686.x
Fang, K.-P., Nan, F.-R., Feng, J., Lv, J.-P., Liu, Q. & Xie, S.-L. (2019) Morphology and molecular phylogeny of a freshwater red algae. Journal of Lake Sciences 31 (1): 220–235. https://doi.org/10.18307/2019.0121
Fischer, E., Gerlach, J., Killmann, D. & Quandt, D. (2020) The freshwater red algae (Batrachospermales, Rhodophyta) of Africa and Madagascar I. New species of Kumanoa, Sirodotia and the new genus Ahidranoa (Batrachospermaceae). Plant and Fungal Systematics 65 (1): 147–166. https://doi.org/10.35535/pfsyst-2020-0010
Freshwater, D.W. & Rueness, J. (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33 (3): 187–194. https://doi.org/10.2216/i0031-8884-33-3-187.1
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59 (3): 307–321. https://doi.org/10.1093/sysbio/syq010
Guiry, M.D. & Guiry, G.M. (2021) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org (accessed 30 April 2021)
Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignment program for windows 95/98/NT. Nucleic Acids Symposium Series 41 (41): 95–98. https://doi.org/10.1021/bk-1999-0734.ch008
Jao, C.-C. (1941) Studies on the freshwater algae of China. VIII. A preliminary account of the Chinese freshwater Rhodophyceae. Sinesia, 12: 245–289.
Ji, L., Xie, S.-L., Feng, J., Chen, L. & Wang, J. (2014) Molecular systematics of the four endemic Batrachospermaceae (Rhodophyta) species in China with multilocus data. Journal of Sytematics Evolution 52 (1): 92–100. https://doi.org/10.1111/jse.12058
Johnston, E.T., Lim, P.E., Buhari, N., Keil, E.J., Djawad, M.I. & Vis, M.L. (2014) Diversity of freshwater red algae (Rhodophyta) in Malaysia and Indonesia from morphological and molecular data. Phycologia 53 (4): 329–341. https://doi.org/10.2216/13-223.1
Kumano, S. (2002) Freshwater Red Algae of the World. Biopress Ltd, Bristol, UK, pp. 1–375.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution formolecular and morphological phylogenetic analyses. Molecular biology and evolution 34 (3): 772–773. https://doi.org/dx.doi.org/10.1093/molbev/msw260
Li, Q., Ji, L. & Xie, S.L. (2010) Phylogenetic analysis of Batrachospemales (Florideophyceae, Rhodophyta) based on chloroplast rbcL sequences. Acta Hydrobiologica Sinica 34 (1): 20–28. https://doi.org/10.3724/sp.j.1035.2010.00020
Minh, B.Q., Nguyen, M. & Haeseler, A.V. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30 (5): 1188–1195. https://doi.org/10.1093/molbev/mst024
Nan, F.-R., Feng, J. & Xie, S.-L. (2014) Phylogenetic relationship of genus Kumanoa (Batrachospermales, Rhodophyta) based on UPA genes. Bulletin of Botanical Research 34 (5): 584–591. https://doi.org/CNKI:SUN:MBZW.0.2014-05-002
Nan, F.-R., Feng, J. & Xie, S.-L. (2015) Phylogenetic relationship of genus Kumanoa based on chloroplast psaA and psbA genes. Acta Phytotaxonomica Sinica 39 (1): 155–163. https://doi.org/10.7541/2015.20
Necchi, O.Jr. & Vis, M.L. (2012) Monograph of the genus Kumanoa (Rhodophyta, Batrachospermales). Bibliothece Phycologica 116: 1–79.
Necchi, O.Jr., Vis, M.L. & Oliveira, M.C. (2010) Phylogenetic relationships in Kumanoa (Batrachospermales, Rhodophyta) species in Brazil with the proposal of Kumanoa amazonensis sp nov. Phycologia 49 (1): 97–103. https://doi.org/10.2216/09-24.1
Necchi, O.Jr., Agostinho, D.C. & Vis, M.L. (2018) Revision of Batrachospermum section Virescentia (Batrachospermales, Rhodophyta) with the establishment of the new genus, Virescentia stat. nov.. Cryptogamie Algologie 39 (3): 313–338. https://doi.org/10.7872/crya/v39.iss3.2018.313
Necchi, O.Jr., Garcia, Fo.A.S. & Paiano, M.O. (2019a) Revision of Batrachospermum sections Acarposporophytum and Aristata (Batrachospermales, Rhodophyta) with the establishment of the new genera Acarposporophycos and Visia. Phytotaxa 395 (2): 51–65. https://doi.org/10.11646/phytotaxa.395.2.1
Necchi, O.Jr., Garcia, Fo.A.S., Paiano, M.O. & Vis, M.L. (2019b) Revision of Batrachospermum section Macrospora (Batrachospermales, Rhodophyta) with the establishment of the new genus Montagnia. Phycologia 58 (6): 582–591. https://doi.org/10.1080/00318884.2019.1624143
Nguyen, L.T., Schmidt, H.A., Haeseler, A.V. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology & Evolution 32 (1): 268–274. https://doi.org/10.1093/molbev/msu300
Ronquist, F., Teslenko, M., Van, Der. Mark, P., Ayres, D.L., Dar, L.A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
Salomaki, E.D., Kwandrans, J., Eloranta, P. & Vis, M.L. (2014) Molecular and morphological evidence for Sheathia gen. nov. (Batrachospermales, Rhodophyta) and three new species. Journal of Phycology 50 (3): 526–542. https://doi.org/10.1111/jpy.12179
Saunders, G.W. (1993) Gel purification of red algal genomic DNA: an inexpensive and rapid method for the isolation of polymerase chain reaction-friendly DNA. Journal of Phycology 29 (2): 251–254. https://doi.org/10.1111/j.0022-3646.1993.00251.x
Saunders, G.W. (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philosophical transactions of the Royal Society B. Biological sciences 360 (1462): 1879–1888. http://dx.doi.org/10.1098/rstb.2005.1719
Saunders, G.W. & 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 (1): 31–43. https://doi.org/10.4490/algae.2013.28.1.031
Sherwood, A.R., Jones, C.A. & Conklin, K.Y. (2014) A New Species of Kumanoa (Batrachospermales, Rhodophyta) from Kôke‘e State Park, Kaua‘i, Hawai‘i,” Pacific Science 68 (4): 577–585. https://doi.org/10.2984/68.4.11
Shi, Z.-X. (1994) Two New Species of the Genus Batrachospermum (Rhodophyta) in China. Acta Phytotaxonomica Sinica 32 (3): 275–280. http://dx.doi.org/10.1080/09397140.2002.10637945
Szinte, A.L., Taylor, J.C., Abosede, A.T. & Vis, M.L. (2020) Current status of freshwater red algal diversity (Rhodophyta) of the African continent including description of new taxa (Batrachospermales). Phycologia 59 (3): 187–199. https://doi.org/10.1080/00318884.2020.1732149
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28 (10): 2731–2739. http://doi.org/10.1093/molbev/msr121
Thiers, B. (2021) [continuously updated] Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium, New York. Available from: http://sweetgum.nybg.org/ih/ (accessed 24 March 2021)
Vis, M.L. & Sheath, R.G. (1997) Biogeography of Batrachospermum gelatinosum (Batrachospermales, Rhodophyta) in North America based on molecular and morphological data. Journal of Phycology 33 (3): 520–526. https://doi.org/10.1111/j.0022-3646.1997.00520.x
Vis, M.L., Necchi, O.Jr., Chiasson, W.B. & Entwisle, T.J. (2012) Molecular phylogeny of the genus Kumanoa (Batrachospermales, Rhodophyta). Journal of Phycology 48 (3): 750–758. https://doi.org/10.1111/j.1529-8817.2012.01141.x
Vis, M.L., Lee, J., Eloranta, P., Chapuis, I.S., Lam, D.W. & Necchi, O.Jr. (2020) Paludicola gen. nov. and revision of the species formerly in Batrachospermum Section Turfosa (Batrachospermales, Rhodophyta). Journal of Phycology 56 (4): 844–861. http://dx.doi.org/10.1111/jpy.13001
Xie, S.-L. & Shi, Z.-X. (2003) New reports of Batrachospermum Roth (Batrachospermales, Rhodophyta) from China. Bulletin of Botanical Research 23 (3): 269–275.
Xie, S.-L. & Shi, Z.-X. (2005) Three new species of Batrachospermum Roth (Batrachospermaceae, Rhodophyta) in China. Chinese Journal of Oceanology & Limnology 23 (2): 204–209. https://doi.org/10.1007/BF02894240
Xie, S.-L., Shi, Z.-X., Lu, H.-S. & Liang, L.-B. (2003) Four new reports of Batrachospermum (Batrachospermales, Rhodophyta) from china. Journal of Wuhan Botanical Research 21 (2): 148–152. https://doi.org/10.1023/A:1022289509702
Xie, S.-L., Qiu, M.-Y., Nan, F.-R., Fang, K.-P. & Han, J.-F. (2020) Batrachospermales (Rhodophyta) of China: a catalogue and bibliography. Nova Hedwigia 110 (1–2): 37–77. https://doi.org/10.1127/nova_hedwigia/2020/0565
Zhang, D., Gao. F, Jakovli?, I., Zou, H., Zhang, J., Li, W.X. & Wang, G.T. (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20 (1): 348–355. https://doi.org/10.1111/1755-0998.13096
Fang, K.-P., Nan, F.-R., Feng, J., Lv, J.-P., Liu, Q. & Xie, S.-L. (2019) Morphology and molecular phylogeny of a freshwater red algae. Journal of Lake Sciences 31 (1): 220–235. https://doi.org/10.18307/2019.0121
Fischer, E., Gerlach, J., Killmann, D. & Quandt, D. (2020) The freshwater red algae (Batrachospermales, Rhodophyta) of Africa and Madagascar I. New species of Kumanoa, Sirodotia and the new genus Ahidranoa (Batrachospermaceae). Plant and Fungal Systematics 65 (1): 147–166. https://doi.org/10.35535/pfsyst-2020-0010
Freshwater, D.W. & Rueness, J. (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33 (3): 187–194. https://doi.org/10.2216/i0031-8884-33-3-187.1
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59 (3): 307–321. https://doi.org/10.1093/sysbio/syq010
Guiry, M.D. & Guiry, G.M. (2021) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org (accessed 30 April 2021)
Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignment program for windows 95/98/NT. Nucleic Acids Symposium Series 41 (41): 95–98. https://doi.org/10.1021/bk-1999-0734.ch008
Jao, C.-C. (1941) Studies on the freshwater algae of China. VIII. A preliminary account of the Chinese freshwater Rhodophyceae. Sinesia, 12: 245–289.
Ji, L., Xie, S.-L., Feng, J., Chen, L. & Wang, J. (2014) Molecular systematics of the four endemic Batrachospermaceae (Rhodophyta) species in China with multilocus data. Journal of Sytematics Evolution 52 (1): 92–100. https://doi.org/10.1111/jse.12058
Johnston, E.T., Lim, P.E., Buhari, N., Keil, E.J., Djawad, M.I. & Vis, M.L. (2014) Diversity of freshwater red algae (Rhodophyta) in Malaysia and Indonesia from morphological and molecular data. Phycologia 53 (4): 329–341. https://doi.org/10.2216/13-223.1
Kumano, S. (2002) Freshwater Red Algae of the World. Biopress Ltd, Bristol, UK, pp. 1–375.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution formolecular and morphological phylogenetic analyses. Molecular biology and evolution 34 (3): 772–773. https://doi.org/dx.doi.org/10.1093/molbev/msw260
Li, Q., Ji, L. & Xie, S.L. (2010) Phylogenetic analysis of Batrachospemales (Florideophyceae, Rhodophyta) based on chloroplast rbcL sequences. Acta Hydrobiologica Sinica 34 (1): 20–28. https://doi.org/10.3724/sp.j.1035.2010.00020
Minh, B.Q., Nguyen, M. & Haeseler, A.V. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30 (5): 1188–1195. https://doi.org/10.1093/molbev/mst024
Nan, F.-R., Feng, J. & Xie, S.-L. (2014) Phylogenetic relationship of genus Kumanoa (Batrachospermales, Rhodophyta) based on UPA genes. Bulletin of Botanical Research 34 (5): 584–591. https://doi.org/CNKI:SUN:MBZW.0.2014-05-002
Nan, F.-R., Feng, J. & Xie, S.-L. (2015) Phylogenetic relationship of genus Kumanoa based on chloroplast psaA and psbA genes. Acta Phytotaxonomica Sinica 39 (1): 155–163. https://doi.org/10.7541/2015.20
Necchi, O.Jr. & Vis, M.L. (2012) Monograph of the genus Kumanoa (Rhodophyta, Batrachospermales). Bibliothece Phycologica 116: 1–79.
Necchi, O.Jr., Vis, M.L. & Oliveira, M.C. (2010) Phylogenetic relationships in Kumanoa (Batrachospermales, Rhodophyta) species in Brazil with the proposal of Kumanoa amazonensis sp nov. Phycologia 49 (1): 97–103. https://doi.org/10.2216/09-24.1
Necchi, O.Jr., Agostinho, D.C. & Vis, M.L. (2018) Revision of Batrachospermum section Virescentia (Batrachospermales, Rhodophyta) with the establishment of the new genus, Virescentia stat. nov.. Cryptogamie Algologie 39 (3): 313–338. https://doi.org/10.7872/crya/v39.iss3.2018.313
Necchi, O.Jr., Garcia, Fo.A.S. & Paiano, M.O. (2019a) Revision of Batrachospermum sections Acarposporophytum and Aristata (Batrachospermales, Rhodophyta) with the establishment of the new genera Acarposporophycos and Visia. Phytotaxa 395 (2): 51–65. https://doi.org/10.11646/phytotaxa.395.2.1
Necchi, O.Jr., Garcia, Fo.A.S., Paiano, M.O. & Vis, M.L. (2019b) Revision of Batrachospermum section Macrospora (Batrachospermales, Rhodophyta) with the establishment of the new genus Montagnia. Phycologia 58 (6): 582–591. https://doi.org/10.1080/00318884.2019.1624143
Nguyen, L.T., Schmidt, H.A., Haeseler, A.V. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology & Evolution 32 (1): 268–274. https://doi.org/10.1093/molbev/msu300
Ronquist, F., Teslenko, M., Van, Der. Mark, P., Ayres, D.L., Dar, L.A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
Salomaki, E.D., Kwandrans, J., Eloranta, P. & Vis, M.L. (2014) Molecular and morphological evidence for Sheathia gen. nov. (Batrachospermales, Rhodophyta) and three new species. Journal of Phycology 50 (3): 526–542. https://doi.org/10.1111/jpy.12179
Saunders, G.W. (1993) Gel purification of red algal genomic DNA: an inexpensive and rapid method for the isolation of polymerase chain reaction-friendly DNA. Journal of Phycology 29 (2): 251–254. https://doi.org/10.1111/j.0022-3646.1993.00251.x
Saunders, G.W. (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philosophical transactions of the Royal Society B. Biological sciences 360 (1462): 1879–1888. http://dx.doi.org/10.1098/rstb.2005.1719
Saunders, G.W. & 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 (1): 31–43. https://doi.org/10.4490/algae.2013.28.1.031
Sherwood, A.R., Jones, C.A. & Conklin, K.Y. (2014) A New Species of Kumanoa (Batrachospermales, Rhodophyta) from Kôke‘e State Park, Kaua‘i, Hawai‘i,” Pacific Science 68 (4): 577–585. https://doi.org/10.2984/68.4.11
Shi, Z.-X. (1994) Two New Species of the Genus Batrachospermum (Rhodophyta) in China. Acta Phytotaxonomica Sinica 32 (3): 275–280. http://dx.doi.org/10.1080/09397140.2002.10637945
Szinte, A.L., Taylor, J.C., Abosede, A.T. & Vis, M.L. (2020) Current status of freshwater red algal diversity (Rhodophyta) of the African continent including description of new taxa (Batrachospermales). Phycologia 59 (3): 187–199. https://doi.org/10.1080/00318884.2020.1732149
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28 (10): 2731–2739. http://doi.org/10.1093/molbev/msr121
Thiers, B. (2021) [continuously updated] Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium, New York. Available from: http://sweetgum.nybg.org/ih/ (accessed 24 March 2021)
Vis, M.L. & Sheath, R.G. (1997) Biogeography of Batrachospermum gelatinosum (Batrachospermales, Rhodophyta) in North America based on molecular and morphological data. Journal of Phycology 33 (3): 520–526. https://doi.org/10.1111/j.0022-3646.1997.00520.x
Vis, M.L., Necchi, O.Jr., Chiasson, W.B. & Entwisle, T.J. (2012) Molecular phylogeny of the genus Kumanoa (Batrachospermales, Rhodophyta). Journal of Phycology 48 (3): 750–758. https://doi.org/10.1111/j.1529-8817.2012.01141.x
Vis, M.L., Lee, J., Eloranta, P., Chapuis, I.S., Lam, D.W. & Necchi, O.Jr. (2020) Paludicola gen. nov. and revision of the species formerly in Batrachospermum Section Turfosa (Batrachospermales, Rhodophyta). Journal of Phycology 56 (4): 844–861. http://dx.doi.org/10.1111/jpy.13001
Xie, S.-L. & Shi, Z.-X. (2003) New reports of Batrachospermum Roth (Batrachospermales, Rhodophyta) from China. Bulletin of Botanical Research 23 (3): 269–275.
Xie, S.-L. & Shi, Z.-X. (2005) Three new species of Batrachospermum Roth (Batrachospermaceae, Rhodophyta) in China. Chinese Journal of Oceanology & Limnology 23 (2): 204–209. https://doi.org/10.1007/BF02894240
Xie, S.-L., Shi, Z.-X., Lu, H.-S. & Liang, L.-B. (2003) Four new reports of Batrachospermum (Batrachospermales, Rhodophyta) from china. Journal of Wuhan Botanical Research 21 (2): 148–152. https://doi.org/10.1023/A:1022289509702
Xie, S.-L., Qiu, M.-Y., Nan, F.-R., Fang, K.-P. & Han, J.-F. (2020) Batrachospermales (Rhodophyta) of China: a catalogue and bibliography. Nova Hedwigia 110 (1–2): 37–77. https://doi.org/10.1127/nova_hedwigia/2020/0565
Zhang, D., Gao. F, Jakovli?, I., Zou, H., Zhang, J., Li, W.X. & Wang, G.T. (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20 (1): 348–355. https://doi.org/10.1111/1755-0998.13096