The model marine diatom Thalassiosira pseudonana likely descended from a freshwater ancestor in the genus Cyclotella

BMC Evolutionary Biology

Edward C Theriot⁴  Matthew L Julius¹  Bánk Beszteri³  Andrew J Alverson² 

[1] St. Cloud State University, Department of Biological Sciences, 720 Fourth Avenue South, St. Cloud, MN 56301, USA;Indiana University, Department of Biology, 1001 East Third Street, Bloomington, IN 47405, USA;Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany;The University of Texas at Austin, Texas Natural Science Center, 2400 Trinity Street, Austin, TX 78705, USA

关键词: Thalassiosira pseudonana;    model species;    marine;    freshwater;    diatom;    Cyclotella nana;   

Others  :  1144408
DOI  :  10.1186/1471-2148-11-125

 received in 2010-12-20, accepted in 2011-05-14,  发布年份 2011

【 摘 要 】

Background

Publication of the first diatom genome, that of Thalassiosira pseudonana, established it as a model species for experimental and genomic studies of diatoms. Virtually every ensuing study has treated T. pseudonana as a marine diatom, with genomic and experimental data valued for their insights into the ecology and evolution of diatoms in the world's oceans.

Results

The natural distribution of T. pseudonana spans both marine and fresh waters, and phylogenetic analyses of morphological and molecular datasets show that, 1) T. pseudonana marks an early divergence in a major freshwater radiation by diatoms, and 2) as a species, T. pseudonana is likely ancestrally freshwater. Marine strains therefore represent recent recolonizations of higher salinity habitats. In addition, the combination of a relatively nondescript form and a convoluted taxonomic history has introduced some confusion about the identity of T. pseudonana and, by extension, its phylogeny and ecology. We resolve these issues and use phylogenetic criteria to show that T. pseudonana is more appropriately classified by its original name, Cyclotella nana. Cyclotella contains a mix of marine and freshwater species and so more accurately conveys the complexities of the phylogenetic and natural histories of T. pseudonana.

Conclusions

The multitude of physical barriers that likely must be overcome for diatoms to successfully colonize freshwaters suggests that the physiological traits of T. pseudonana, and the genes underlying those traits, might differ from those of strictly marine diatoms. The freshwater ancestry of T. pseudonana might therefore confound generalizations about the physiological and metabolic properties of marine diatoms. The freshwater component of T. pseudonana's history merits careful consideration in the interpretation of experimental data collected for this important model species.

【 授权许可】

   
2011 Alverson et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

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【 参考文献 】

• [1]Archibald JM: The puzzle of plastid evolution. Curr Biol 2009, 19(2):R81-R88.
• [2]Mann DG, Droop SJM: Biodiversity, biogeography and conservation of diatoms. Hydrobiologia 1996, 336(1-3):19-32.
• [3]Nelson DM, Treguer P, Brzezinski MA, Leynaert A, Queguiner B: Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem Cy 1995, 9(3):359-372.
• [4]Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, et al.: The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 2004, 306(5693):79-86.
• [5]Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D: Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 2009, 324(5935):1724-1726.
• [6]Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, et al.: The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456(7219):239-244.
• [7]Armbrust EV, Rynearson TA, Jenkins BD: Genomic insights into diatom evolution and metabolism. In Genomics and Evolution of Microbial Eukaryotes. Edited by Katz LA, Bhattacharya D. Oxford: Oxford Univeristy Press; 2006:201-213.
• [8]Guillard RRL, Kilham P, Jackson TA: Kinetics of silicon-limited growth in the marine diatom Thalassiosira pseudonana Hasle and Heimdal (Cyclotella nana Hustedt). J Phycol 1973, 9:233-237.
• [9]Nelson DM, Goering JJ, Kilham SS, Guillard RRL: Kinetics of silicic-acid uptake and rates of silica dissolution in marine diatom Thalassiosira pseudonana. J Phycol 1976, 12(2):246-252.
• [10]Paasche E: Silicon and the ecology of marine plankton diatoms. I Thalassiosira pseudonana (Cyclotella nana) grown in a chemostat with silicate as limiting nutrient. Mar Biol (Berl) 1973, 19:117-126.
• [11]Poulsen N, Chesley PM, Kroger N: Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 2006, 42(5):1059-1065.
• [12]Bowler C, Vardi A, Allen AE: Oceanographic and biogeochemical insights from diatom genomes. Annu Rev Mar Sci 2010, 2:333-365.
• [13]Parker MS, Armbrust EV: Synergistic effects of light, temperature, and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 2005, 41(6):1142-1153.
• [14]Kustka AB, Allen AE, Morel FMM: Sequence analysis and transcriptional regulation of iron acquisition genes in two marine diatoms. J Phycol 2007, 43(4):715-729.
• [15]Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL, Ribalet F, Murphy MEP, Maldonado MT, Armbrust EV: Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 2009, 457(7228):467-470.
• [16]Sumper M, Brunner E: Silica biomineralisation in diatoms: The model organism Thalassiosira pseudonana. ChemBioChem 2008, 9(8):1187-1194.
• [17]Frigeri LG, Radabaugh TR, Haynes PA, Hildebrand M: Identification of proteins from a cell wall fraction of the diatom Thalassiosira pseudonana: Insights into silica structure formation. Mol Cell Proteomics 2005, 5:182-193.
• [18]Mock T, Samanta MP, Iverson V, Berthiaume C, Robison M, Holtermann K, Durkin C, BonDurant SS, Richmond K, Rodesch M, et al.: Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. P Natl Acad Sci USA 2008, 105(5):1579-1584.
• [19]Thamatrakoln K, Hildebrand M: Analysis of Thalassiosira pseudonana silicon transporters indicates distinct regulatory levels and transport activity through the cell cycle. Eukaryot Cell 2007, 6(2):271-279.
• [20]Parker MS, Mock T, Armbrust EV: Genomic insights into marine microalgae. Annu Rev Genet 2008, 42:619-645.
• [21]Finlay BJ, Monaghan EB, Maberly SC: Hypothesis: The rate and scale of dispersal of freshwater diatom species is a function of their global abundance. Protist 2002, 153(3):261-273.
• [22]Julius ML, Tanimura Y: Cladistic analysis of plicated Thalassiosira (Bacillariophyceae). Phycologia 2001, 40(2):111-122.
• [23]Johansen J, Kociolek P, Lowe R: Spicaticribra kingstonii, gen. nov. et sp. nov. (Thalassiosiraceae, Bacillariophyta) from Great Smoky Mountains National Park, USA. Diatom Res 2008, 23(2):367-375.
• [24]Stachura-Suchoples K, Williams DM: Description of Conticribra tricircularis, a new genus and species of Thalassiosirales, with a discussion on its relationship to other continuous cribra species of Thalassiosira Cleve (Bacillariophyta) and its freshwater origin. Eur J Phycol 2009, 44(4):477-486.
• [25]Alverson AJ, Jansen RK, Theriot EC: Bridging the Rubicon: Phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Mol Phylogenet Evol 2007, 45(1):193-210.
• [26]Chang TP, Chang-Scheider H: Zentrische kieselalgen in Kemptener seen [Centric diatoms in lakes of Kempten]. Ber Deut Bot Ges 2008, 78:5-15.
• [27]Chang TP, Steinberg C: Identifizierung von nanoplanktischen Kieselalgen (Centrales, Bacillariophyceae) in der Rott und im Rott-Stausee (Bayern, Bundesrepublik Deutschland) [Identification of nanoplanktonic diatoms (Centrales, Bacillariophyceae) in River Rott and Rott Reservoir (Bavaria, F.R.G.)]. Arch Protistenkd 1989, 137(2):111-129.
• [28]Hasle GR, Heimdal BR: Some species of the centric diatom genus Thalassiosira studied in the light and electron microscopes. Beihefte zur Nova Hedwigia 1970, 31:543-581.
• [29]Hustedt F: Die Diatomeenflora des Flußsystems der Weser im Gebiet der Hansestadt Bremen [Diatom flora of the tributaries of the Weser near the city of Bremen]. Abh Naturw Ver Bremen 1957, 34:181-440.
• [30]Guillard RRL, Ryther JH: Studies of marine planktonic diatoms. I Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 1962, 8:229-239.
• [31]Belcher JH, Swale EMF: Species of Thalassiosira (Diatoms, Bacillariophyceae) in the plankton of English rivers. Br Phycol J 1977, 12(3):291-297.
• [32]Hasle GR: The marine, planktonic diatoms Thalassiosira oceanica sp. nov. and T. partheneia. J Phycol 1983, 19(2):220-229.
• [33]Hustedt F: Die Diatomeenflora der Unterweser von der Lesummündung bis Bremerhaven mit Berücksichtigung des Unterlaufs der Hunte und Geeste [Diatom flora of the lower Weser from the Lesum estuary to Bremerhaven, with consideration of the lower Hunte and Geeste]. Veröff Inst Meeresforsch 1959, 6:13-176.
• [34]Lowe RL: Comparative ultrastructure of the valves of some Cyclotella species (Bacillariophyceae). J Phycol 1975, 11(4):415-424.
• [35]Fryxell GA, Hasle GR: Thalassiosira eccentrica (Ehrenb.) Cleve, T. symmetrica sp. nov., and some related centric diatoms. J Phycol 1972, 8:297-317.
• [36]Fryxell GA, Hasle GR: The genus Thalassiosira: some species with a modified ring of central strutted processes. Beiheft zur Nova Hedwigia 1977, 54:67-98.
• [37]Fryxell GA, Hasle GR: The genus Thalassiosira: species with internal extensions of the strutted processes. Phycologia 1979, 18(4):378-393.
• [38]Hasle GR: Some Thalassiosira species with one central process. Norwegian Journal of Botany 1978, 25:77-110.
• [39]Hasle GR, Fryxell GA: The genus Thalassiosira: some species with a linear areola array. Nova Hedwigia Beih 1977, 54:14-60.
• [40]Hasle GR, Lange CB: Freshwater and brackish water Thalassiosira (Bacillariophyceae) taxa with tangentially undulated valves. Phycologia 1989, 28(1):120-135.
• [41]Håkansson H: A compilation and evaluation of species in the general Stephanodiscus, Cyclostephanos and Cyclotella with a new genus in the family Stephanodiscaceae. Diatom Res 2002, 17(1):1-139.
• [42]Loginova LP: Classification of the diatom genus Cyclotella. In Proceedings of the 10th International Symposium on Recent and Fossil Diatoms. Edited by Simola H. Koenigstein: Otto Koeltz Science Publishers; 1990:37-46.
• [43]Serieyssol KK: Cyclotella species of late Miocene age from St. Bauzile, France. In Proceedings of the Sixth Symposium on Recent and Fossil Diatoms. Edited by Ross R. Koenigstein: Otto Koeltz Science Publishers; 1980:27-42.
• [44]Pisani D, Benton MJ, Wilkinson M: Congruence of morphological and molecular phylogenies. Acta Biotheor 2007, 55(3):269-281.
• [45]von Dassow P, Petersen TW, Chepurnov VA, Armbrust EV: Inter- and intraspecific relationships between nuclear DNA content and cell size in selected members of the centric diatom genus Thalassiosira (Bacillariophyceae). J Phycol 2008, 44(2):335-349.
• [46]Maldonado MT, Allen AE, Chong JS, Lin K, Leus D, Karpenko N, Harris SL: Copper-dependent iron transport in coastal and oceanic diatoms. Limnol Oceanogr 2006, 51(4):1729-1743.
• [47]Strzepek RF, Harrison PJ: Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 2004, 431(7009):689-692.
• [48]Wetzel RG: Iron, sulfur, and silica cycles. In Limnology: Lake and River Ecosystems. Third edition. San Diego: Academic Press; 2001:289-331.
• [49]Sunda WG, Huntsman SA: Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem 1995, 50(1-4):189-206.
• [50]De Martino A, Meichenin A, Shi J, Pan KH, Bowler C: Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. J Phycol 2007, 43(5):992-1009.
• [51]Round FE, Sims PA: The distribution of diatom genera in marine and freshwater environments and some evolutionary considerations. In Proceedings of the Sixth Symposium on Recent and Fossil Diatoms. Edited by Ross R. Hirschberg: Otto Koeltz Science Publishers; 1980:301-320.
• [52]Shapiro B, Rambaut A, Drummond AJ: Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 2006, 23(1):7-9.
• [53]Wilgenbusch JC, Warren DL, Swofford DL: AWTY: A system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. 2004.