Browse > Article
http://dx.doi.org/10.4490/algae.2014.29.2.057

Phylogenetic position of eight Amphora sensu lato (Bacillariophyceae) species and comparative analysis of morphological characteristics  

Wang, Pengbin (Department of Life Science, College of Natural Sciences, Hanyang University)
Park, Bum Soo (Department of Life Science, College of Natural Sciences, Hanyang University)
Kim, Jin Ho (Department of Life Science, College of Natural Sciences, Hanyang University)
Kim, Joo-Hwan (Department of Life Science, College of Natural Sciences, Hanyang University)
Lee, Hae-Ok (Department of Life Science, College of Natural Sciences, Hanyang University)
Han, Myung-Soo (Department of Life Science, College of Natural Sciences, Hanyang University)
Publication Information
ALGAE / v.29, no.2, 2014 , pp. 57-73 More about this Journal
Abstract
Amphora Ehrenberg ex Kutzing sensu lato is a common and widespread benthic diatom genus with a taxonomy that has been under continual revision, particularly based on molecular analyses. Although Amphora species have been studied using modern microscopy in recent years, there has not been much progress on molecular characterization of the species, especially in Asia. In this study of Amphora, sampling was carried out from September 2009 to August 2010 in Korean coastal waters. The morphological and molecular characteristics of eight Amphora sensu lato were examined: Amphora marina, A. proteus, Halamphora costata, H. coffeaeformis, H. eunotia, H. holsatica, H. terroris, and Halamphora sp. Based on previous accounts, morphology suggested that A. marina and A. proteus belong to the subgenus Amphora Cleve, which have smooth girdle bands and rather coarse and very distinct areolae on the valve. The other species, H. coffeaeformis, H. costata, H. eunotia, H. holsatica, H. terroris, and Halamphora sp. belong to the subgenus Halamphora Cleve, which was recently elevated to generic status by Levkov 2009, have plicate girdle bands, puncta which do not form straight longitudinal lines, valves which have a narrow ventral portion and apices that are generally rostrate-capitate and recurved. In agreement with analysis based on morphological characteristics, phylogenetic analysis based on small subunit rDNA suggested that the eight Amphora sensu lato species were not a monophyletic group as the morphological classification. Also, the results of molecular work and statistical analysis on all these Amphora sensu lato combined with phylogenic analysis on our geographically representative samples give strong evidence that Halamphora Levkov is independent of Amphora Cleve. Furthermore, in this study, Amphora terroris was transferred Halamphora as Halamphora terroris (Ehrenberg) Wang comb. nov. and Amphora marina was recorded for the first time in Korea.
Keywords
diatom; molecular phylogeny; morphology; nuclear DNA; taxonomy;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Sato, S., Tamotsu, N. & Mann, D. G. 2013. Morphology and life history of Amphora commutata (Bacillariophyta) I: the vegetative cell and phylogenetic position. Phycologia 52:225-238.   DOI
2 Schmidt, A. & Fricke, F. 1875. Atlas der Diatomaceen-kunde. C. H. Kain, London, 95 pp.
3 Schoeman, F. R. & Archibald, R. E. M. 1976. The diatom flora of Southern Africa: National Institute for water research, CSIR Special Report. Council for Scientific and Industrial Research, Pretoria, 62 pp.
4 Smith, W. 1857. Notes of an excursion to the Pyrenees in search of Diatomaceae. Ann. Mag. Nat. Hist. Ser. 2 19:1-13.
5 Smith, W. & West, T. 1853. A synopsis of the British Diatomaceae: with remarks on their structure, functions and distribution; and instructions for collecting and preserving specimens. J. Van Voorst, London, 86 pp.
6 Posada, D. & Buckley, T. R. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53:793-808.   DOI   ScienceOn
7 Rabenhorst, L. 1868. Flora europaea algarum aquae dulcis et submarinae. E. Kummerum, Leipzig, 359 pp.
8 Mann, D. G. & Poulickova, A. 2010. Mating system, auxosporulation, species taxonomy and evidence for homoploid evolution in Amphora (Bacillariophyta). Phycologia 49:183-201.   DOI
9 Tomas, C. R. 1996. Identifying marine diatoms and dinoflagellates. Academic Press, San Diego, CA, 858 pp.
10 Van Heurck, H. 1896. A treatise on the Diatomaceae. W. E. Baxter Ltd., London, 559 pp.
11 Vesela, J., Neustupa, J., Pichrtova, M. & Poulickova, A. 2009. Morphometric study of Navicula morphospecies (Bacillariophyta) with respect to diatom life cycle. Fottea 9:307-316.
12 Wasell, A. & Hakansson, H. 1992. Diatom stratigraphy in a lake on Horseshoe island, Antarctica: a marine-brackish-fresh water transition with comments on the systematics and ecology of the most common diatoms. Diatom Res. 7:157-194.   DOI
13 Wehr, J. D. & Sheath, R. G. 2003. Freshwater algae of North America: ecology and classification. Academic Press, San Diego, CA, 917 pp.
14 Ki, J. -S., Cho, S. -Y., Katano, T., Jung, S. W., Lee, J., Park, B. S., Kang, S. -H. & Han, M. -S. 2009. Comprehensive comparisons of three pennate diatoms, Diatoma tenuae, Fragilaria vaucheriae, and Navicula pelliculosa, isolated from summer Arctic reservoirs (Svalbard $79^{\circ}N$), by fine-scale morphology and nuclear 18S ribosomal DNA. Polar Biol. 32:147-159.   DOI   ScienceOn
15 Wolle, F. 1894. Diatomaceae of North America: illustrated with twenty-three hundred figures from the author's drawings on one hundred and twelve plate. The Comenius Press, Bethlehem, PA, 506 pp.
16 Wood, E. J. F. & Crosby, L. 1959. Studies on Australian and New Zealand diatoms II. Normally epontic and benthic genera. Trans. R. Soc. N. Z. 86:1-58.
17 Kooistra, W. H. & Medlin, L. K. 1996. Evolution of the diatoms (Bacillariophyta). IV. A reconstruction of their age from small subunit rRNA coding regions and the fossil record. Mol. Phylogenet. Evol. 6:391-407.   DOI   ScienceOn
18 Ki, J. -S. & Han, M. S. 2007. Informative characteristics of 12 divergent domains in complete large subunit rDNA sequences from the harmful dinoflagellate genus, Alexandrium (Dinophyceae). J. Eukaryot. Microbiol. 54:210-219.   DOI   ScienceOn
19 Klipp, E., Liebermeister, W., Wierling, C., Kowald, A., Lehrach, H. & Herwig, R. 2009. Systems biology: a textbook. Wiley-VCH, Weinheim, 592 pp.
20 Krammer, K. 1980. Morphologic and taxonomic investigations of some freshwater species of the diatom genus Amphora Ehr. Bacillaria 3:197-225.
21 Krammer, K., Lange-Bertalot, H., Ettle, H., Gerloff, J., Heyning, H. & Mollenhauer, D. 1991. Bacillariophyceae. Vol. 2/1. Naviculaceae. Gustav Fischer Verlag, Stuttgart and Jena, 876 pp.
22 Mann, D. G. 1993. Patterns of sexual reproduction in diatoms. Hydrobiologia 269/270:11-20.   DOI
23 Kutzing, F. T. 1844. Die Kieselschaligen Bacillarien oder Diatomeen. Zu finden bei W. Kohne, Nordhausen, pp. 1-152.
24 Lee, K. & Round, F. E. 1987. Studies on freshwater Amphora species. I: Amphora ovalis. Diatom Res. 2:193-203.   DOI
25 Levkov, Z. 2009. Diatoms of Europe. Vol. 5. Amphora sensu lato. Koeltz, Koenigstein, 916 pp.
26 Hustedt, F. 1930. Bacillariophyta (Diatomeae). In Pascher, A. (Ed.) Die Susswasser-Flora Mitteleuropas. Heft 10. Zweite Auflage. Gustav Fischer, Jena, pp. 1-466.
27 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. Syst. Biol. 59:307-321.   DOI   ScienceOn
28 Hendey, N. 1964. An introductory account of the smaller algae of British coastal waters. Part V. Bacillariophyceae (diatoms). Her Majesty's Stationary Office, London, 317 pp.
29 Hustedt, F. 1925. Bacillariales aus den Salzgewassern bei Oldesloe in Holstein. Mitteilungen der Geographischen Gesellschaft und der Naturhistorischen Museums in Lubeck, zweite Reihe 30:84-121.
30 Jin, D., Cheng, Z., Lin, J. & Liu, S. 1982. The marine benthic diatoms in China. China Ocean Press, Beijing, 321 pp.
31 Jung, S. W., Han, M. -S. & Ki, J. -S. 2010. Molecular genetic divergence of the centric diatom Cyclotella and Discostella (Bacillariophyceae) revealed by nuclear ribosomal DNA comparisons. J. Appl. Phycol. 22:319-329.   DOI   ScienceOn
32 Chin, T. G., Cheng, Z., Liu, S. & Ma, J. 1992. The marine benthic diatoms in China. China Ocean Press, Beijing, 429 pp.
33 Katano, T., Lee, J., Ki, J. -S., Kang, S. -H. & Han, M. -S. 2007. Effects of temperature and salinity on the growth and the optimum nitrogen to phosphorus ratio for the culture of Diatoma tenue isolated from a temporary arctic pond in Svalbard, Norway. J. Freshw. Ecol. 22:629-635.   DOI   ScienceOn
34 Ki, J. -S., Chang, K. B., Roh, H. J., Lee, B. Y., Yoon, J. Y. & Jang, G. Y. 2007. Direct DNA isolation from solid biological sources without pretreatments with proteinase-K and/or homogenization through automated DNA extraction. J. Biosci. Bioeng. 103:242-246.   DOI   ScienceOn
35 Cleve, P. T. 1873. On diatoms from the Arctic Sea. Bih. K. Sven. Vetensk.-Akad. Handl. 13:1-28.
36 Clavero, E., Grimalt, J. O. & Hernandez-Marine, M. 2000. The fine structure of two small Amphora species. A. tenerrima Aleem & Hustedt and A. tenuissima Hustedt. Diatom Res. 15:195-208.   DOI
37 Cleve-Euler, A. 1953. Die Diatomeen von Schweden und Finnland. III. K. Sven. Vetensk.-Akad. Handl. Ser. IV 4:1-255.
38 Cleve, P. T. 1895. Synopsis of the naviculoid diatoms. K. Sven. Vetensk.-Akad. Handl. 27:99-142.
39 Damste, J. S., Muyzer, G., Abbas, B., Rampen, S. W., Masse, G., Allard, W. G., Belt, S. T., Robert, J. M., Rowland, S. J., Moldowan, J. M., Barbanti, S. M., Fago, F. J., Denisevich, P., Dahl, J., Trindade, L. A. & Schouten, S. 2004. The rise of the rhizosolenid diatoms. Science 304:584-587.   DOI   ScienceOn
40 Davidovich, N. A., Gastineau, R., Gaudin, P., Davidovich, O. I. & Mouget, J. -L. 2012. Sexual reproduction in the newly-described blue diatom, Haslea karadagensis. Fottea 12:219-229.
41 Andersen, R. A. 2005. Algal culturing techniques. Academic Press, San Diego, CA, 578 pp.
42 Ehrenberg, C. G. 1853. Uber einige neue Materialien zur Ubersicht des kleinsten Lebens. Bericht uber die zur Bekanntmachung geeigneten Verhandlungen der Koniglich-Preussischen Akademie der Wissenschaften zu Berlin 1853:505-533.
43 Gregory, W. 1857. On new forms of marine Diatomaceae found in the Firth of Clyde and in Loch Fyne, illustrated by numerous figures drawn by R. K. Greville, LL. D., F. R. S. E. Trans. R. Soc. Edinb. 21:473-542.   DOI
44 Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229-239.   DOI   ScienceOn
45 Oh, H. -Y., Cheon, J. -Y., Lee, J. H., Hur, S. B. & Ki, J. -S. 2010. Nuclear rDNA characteristics for DNA taxonomy of the centric diatom Chaetoceros (Bacillariophyceae). Algae 25:65-70.   과학기술학회마을   DOI   ScienceOn
46 Peragallo, H. & Peragallo, M. 1908. Diatomees marines de France et des districts maritimes voisins. Micrographe-Editeur, a Grez-sur-Loing (S.-et-M.), 491 pp.
47 Agardh, C. 1827. Aufzahlung einiger in den ostreichischen Landern gefundenen neuen Gattungen und Arten von Algen, nebst ihrer Diagnostik und beigefugten Bemerkungen. Flora 10:625-646.
48 Archibald, R. E. M. & Schoeman, F. R. 1984. Amphora coffeaeformis (Agardh) Kutzing: a revision of the species under light and electron microscopy. S. Afr. J. Bot. 3:83-102.
49 Beszteri, B., Acs, E., Makk, J., Kovacs, G., Marialigeti, K. & Kiss, K. T. 2001. Phylogeny of six naviculoid diatoms based on 18S rDNA sequences. Int. J. Syst. Evol. Microbiol. 51:1581-1586.
50 Boyer, C. S. 1916. The Diatomaceae of Philadelphia and vicinity. Press of J. B. Lippincott Company, Philadelphia, PA, 232 pp.
51 Boyer, C. S. 1927. Synopsis of North American Diatomaceae. Part 2. Naviculatae, Surirellatae. Proc. Acad. Nat. Sci. Phil. 79:229-583.
52 Bruder, K. & Medlin, L. K. 2007. Molecular assessment of phylogenetic relationships in selected species/genera in the naviculoid diatoms (Bacillariophyta). I. The genus Placoneis. Nova Hedwigia 85:331-352.   DOI   ScienceOn
53 Bruder, K. & Medlin, L. K. 2008. Morphological and molecular investigations of naviculoid diatoms. II. Selected genera and families. Diatom Res. 23:283-329.   DOI
54 Throndsen, J. 1978. Preservation and storage. In Sournia, A. (Ed.) Phytoplankton Manual. UNESCO, Paris, pp. 69-74.
55 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. Mol. Biol. Evol. 28:2731-2739.   DOI   ScienceOn
56 Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.   DOI   ScienceOn
57 Medlin, L. K., Cooper, A., Hill, C., Wrieden, S. & Wellbrock, U. 1995. Phylogenetic position of the Chromista plastids based on small subunit rRNA coding regions. Curr. Genet. 28:560-565.   DOI
58 Medlin, L. K. & Kaczmarska, I. 2004. Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia 43:245-270.   DOI
59 Medlin, L., Williams, D. M. & Sims, P. A. 1993. The evolution of the diatoms (Bacillariophyta). I. Origin of the group and assessment of the monophyly of its major divisions. Eur. J. Phycol. 28:261-275.   DOI   ScienceOn
60 Medlin, L. K., Kooistra, W. H., Gersonde, R. & Wellbrock, U. 1996. Evolution of the diatoms (Bacillariophyta). II. Nuclear-encoded small-subunit rRNA sequence comparisons confirm a paraphyletic origin for the centric diatoms. Mol. Biol. Evol. 13:67-75.   DOI   ScienceOn
61 Nagumo, T. 2003. Taxonomic studies of the subgenus Amphora Cleve of the genus Amphora (Bacillariophyceae) in Japan. Gebruder Borntraeger Verlagsbuchhandlung, Science Publishers, Stuttgart, 265 pp.
62 Sala, S. E., Sar, E. A., Hinz, F. & Sunesen, I. 2006. Studies on Amphora subgenus Halamphora (Bacillariophyta): the revision of some species described by Hustedt using type material. Eur. J. Phycol. 41:155-167.   DOI   ScienceOn
63 Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D. L., Darling, 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. Syst. Biol. 61:539-542.   DOI   ScienceOn
64 Round, F. E., Crawford, R. M. & Mann, D. G. 1990. The diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge, 747 pp.
65 Sala, S. E., Guerrero, J. M. & Coste, M. 2007. Valve morphology of Amphora chilensis Hustedt (Bacillariophyceae). Nova Hedwigia 85:353-364.   DOI
66 Sar, E. A., Sala, S. E., Hinz, F. & Sunesen, I. 2003. Revision of Amphora holsatica (Bacillariophyceae). Eur. J. Phycol. 38:73-81.   DOI   ScienceOn
67 Krammer, K. & Lange-Bertalot, H. 1986. Subwasserflora von Mitteleuropa, Bd 02/1 Bacillariophyceae 1. Teil: Naviculaceae. Spektrum Akademischer Verlag, Heidelberg Berlin, 876 pp.
68 Beerli, P. 2006. Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341-345.   DOI   ScienceOn
69 Nylander, J. A. A. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala.
70 Swofford, D. L. 2003. PAUP*: Phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer Associates, Sunderland, MA.
71 Tempere, J. & Peragallo, H. 1908. Diatomees du Monde Entier. 2nd ed. Chez J. Tempere, Arcachon, pp. 17-112.