Morphological evolution of silica scales in the freshwater genus Synura (Stramenopiles)
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
33135154
DOI
10.1111/jpy.13093
Knihovny.cz E-resources
- Keywords
- Synura punctulosa, chrysophytes, construction principles, microalgae, molecular, morphology, phylogeny, silica scales, synurophytes, ultrastructure,
- MeSH
- Biological Evolution MeSH
- Phylogeny MeSH
- Stramenopiles * MeSH
- Evolution, Molecular MeSH
- Silicon Dioxide * MeSH
- Fresh Water MeSH
- Fossils MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Names of Substances
- Silicon Dioxide * MeSH
A high degree of morphological variability is expressed between the ornately sculptured siliceous scales formed by species in the chrysophycean genus, Synura. In this study, we aimed to uncover the general principles and trends underlying the evolution of scale morphology in this genus. We assessed the relationships among thirty extant Synura species using a robust molecular analysis that included six genes, coupled with morphological characterization of the species-specific scales. The analysis was further enriched with addition of morphological information from fossil specimens and by including the unique modern species, Synura punctulosa. We inferred the phylogenetic position of the morphologically unique S. punctulosa, to be an ancient Synura lineage related to S. splendida in the section Curtispinae. Some morphological traits, including development of a keel or a labyrinth ribbing pattern on the scale, appeared once in evolution, whereas other structures, such as a hexagonal meshwork pattern, originated independently several times over geologic time. We further uncovered numerous construction principles governing scale morphology and evolution, as follows: (i) scale roundness and pore diameter decreased during evolution; (ii) elongated scales became strengthened by a higher number of struts or ribs; (iii) as a consequence of scale biogenesis, scales with spines possessed smaller basal holes than scales with a keel and; and (iv) the keel area was proportional to scale area, indicating its potential value in strengthening the scale against breakage.
Department of Botany Connecticut College New Londo 06320 4196 Connecticut USA
Department of Botany Faculty of Science Charles University Benátská 2 128 00 Praha 2 Czech Republic
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Ankenbrand, M. J., Keller, A., Wolf, M., Schultz, J. & Förster, F. 2015. ITS2 database V: twice as much. Mol. Biol. Evol. 32:3030-2.
Arbour, J. H. & López-Fernández, H. 2013. Ecological variation in South American geophagine cichlids arose during an early burst of adaptive morphological and functional evolution. Proc. R. Soc. B Biol. Sci. 280:20130849.
Asmund, B. 1968. Studies on chrysophyceae from some ponds and lakes in Alaska. VI. Occurrence of Synura species. Hydrobiologia 31:497-515.
Atkinson, D., Ciotti, B. J. & Montagnes, D. J. S. 2003. Protists decrease in size linearly with temperature: ca. 2.5% C-1. Proc. R. Soc. B Biol. Sci. 270:2605-11.
Balonov, I. M. 1976. Rod Synura Ehr. (Chrysophyta). Biologija, Ekologija, Sistematika. Akad. Nauk. SSSR, Institut Vnutrennich Vod., Trudy. 31:61-82.
Beardall, J. & Raven, J. A. 2004. The potential effects of global change on microalgal photosynthesis, growth and ecology. Phycologia 43:26-40.
Beech, P. L., Wetherbee, R. & Pickett-Heaps, J. D. 1990. Secretion and deployment of bristles in Mallomonas splendens (Synurophyceae). J. Phycol. 26:112-22.
Bismuto, A., Setaro, A., Maddalena, P., De Stefano, L. & De Stefano, M. 2008. Marine diatoms as optical chemical sensors: A time-resolved study. Sens. Actuat. B Chem. 130:396-9.
Boenigk, J., Pfandl, K. & Hansen, P. J. 2006. Exploring strategies for nanoflagellates living in a ‘wet desert’. Aquat. Microb. Ecol. 44:71-83.
Boo, S. M., Kim, H. S., Shin, W., Boo, G. H., Cho, S. M., Jo, B. Y., Kim, J. H. et al. 2010. Complex phylogeographic patterns in the freshwater alga Synura provide new insights into ubiquity vs. endemism in microbial eukaryotes. Mol. Ecol. 19:4328-38.
Brugerolle, G. & Bricheux, G. 1984. Actin microfilaments are involved in scale formation of the chrysomonad cell Synura. Protoplasma 123:203-12.
Brussaard, C. P. 2004. Viral control of phytoplankton populations - a review. J. Eukaryotic Microbiol. 51:125-38.
Castellanos, M. C., Wilson, P., Keller, S. J., Wolfe, A. D. & Thomson, J. D. 2006. Anther evolution: pollen presentation strategies when pollinators differ. Am. Nat. 167:288-96.
Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-52.
Čertnerová, D., Čertner, M. & Škaloud, P. 2019. Molecular phylogeny and evolution of phenotype in silica-scaled chrysophyte genus Mallomonas. J. Phycol. 55:912-23.
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772.
De Stefano, L., Rea, I., Rendina, I., De Stefano, M. & Moretti, L. 2007. Lensless light focusing with the centric marine diatom Coscinodiscus walesii. Opt. Express. 15:18082-8.
De Tommasi, E., Rea, I., Mocella, V., Moretti, L., De Stefano, M., Rendina, I. & De Stefano, L. 2010. Multi-wavelength study of light transmitted through a single marine centric diatom. Opt. Express. 18:12203-12.
Elmer, K. R., Kusche, H., Lehtonen, T. K. & Meyer, A. 2010. Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Phil. Trans. R. Soc. B Biol. Sci. 365:1763-82.
Endler, J. A. & Day, L. B. 2006. Ornament colour selection, visual contrast and the shape ofb colour preference functions in great bowerbirds, Chlamydera nuchalis. Anim. Behav. 72:1405-16.
Feilich, K. L. 2016. Correlated evolution of body and fin morphology in the cichlid fishes. Evolution 70:2247-67.
Fott, B. & Ludvík, J. 1957. Die submikroskopische Struktur der Kieselschuppen bei Synura und ihre Bedeutung fur die Taxonomie der Gattung. Preslia 29:5-16.
Gavrilova, O. V., Nogina, N. V. & Voloshko, L. N. 2005. Scale structures and growth characteristics of Synura petersenii (Synurophyceae) under different pH conditions. Nova Hedwig. Beih. 128:249-56.
Greenwood, A. D. 1967. Scale production in Synura. Proc. R. Microbiol. Soc. 2:380-1.
Gutowski, A. 1996. Temperature dependent variability of scales and bristles of Mallomonas tonsurata Teiling emend. Krieger (Synurophyceae). Nova Hedwig. Beih. 114:125-46.
Hartmann, H. & Steinberg, C. 1986. Mallomonadacean (Chrysophyceae) scales: Early biotic paleoindicators of lake acidification. Hydrobiologia 143:87-91.
Hepperle, D.2004. SeqAssem (C). A sequence analysis tool, contig assembler and trace data visualisation tool for molecular sequences. Available from: https://www.sequentix.de/software_seqassem.php.
Herringer, J. W., Lester, D., Dorrington, G. E. & Rosengarten, G. 2019. Can diatom girdle band pores act as a hydrodynamic viral defense mechanism? J. Biol. Phys. 45:213-34.
Jo, B. Y., Kim, J. I., Škaloud, P., Siver, P. A. & Shin, W. 2016. Multigene phylogeny of Synura (Synurophyceae) and descriptions of four new species based on morphological and DNA evidence. Eur. J. Phycol. 51:413-30.
Jo, B. Y., Shin, W., Boo, S. M., Kim, H. S. & Siver, P. A. 2011. Studies on ultrastructure and three-gene phylogeny of the genus Mallomonas (Synurophyceae). J. Phycol. 47:415-25.
Karp-Boss, L. & Boss, E. 2016. The elongated, the squat and the spherical: selective pressures for phytoplankton shape. In Glibert, P. M. & Kana, T. M. [Eds.] Aquatic Microbial Ecology and Biogeochemistry: A Dual Perspective. Springer, Cham, pp. 25-34.
Katana, A., Kwiatowski, J., Spalik, K., Zakryś, B., Szalacha, E. & Szymańska, H. 2001. Phylogenetic position of Koliella (Chlorophyta) as inferred from nuclear and chloroplast small subunit rDNA. J. Phycol. 37:443-51.
Katoh, K., Rozewicki, J. & Yamada, K. D. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings Bioinf. 20:1160-6.
Kiss, K. T. & Kristiansen, J. 1994. Silica-scaled chrysophytes (Synurophyceae) from some rivers and shallow lakes in Hungary. Hydrobiologia 289:157-62.
Klaveness, D. & Guillard, R. R. 1975. The requirement for silicon in Synura petersenii (Chrysophyceae). J. Phycol. 11:349-55.
Kristiansen, J. 1979. Problems in classification and identification of Synuraceae (Chrysophyceae). Aqua. Sci. 40:310-19.
Kristiansen, J. 2008. Dispersal and biogeography of silica-scaled chrysophytes. In Foissner, W. & Hawksworth, D. L. [Eds.] Protist Diversity and Geographical Distribution. Springer, Dordrecht, The Netherlands, pp. 185-192.
Kristiansen, J. & Preisig, H. R. 2007. Chrysophyte and haptophyte algae, part 2: Synurophyceae. In Budel, B., Gärtner, G., Krienitz, L. & Preisig, H. R. [Eds.] Süsswasserflora von Mitteleuropa, vol. 1-2. Springer, Spektrum Akad. Verlag, Berlin, Germany, p. 252.
Kynčlová, A., Škaloud, P. & Škaloudová, M. 2010. Unveiling hidden diversity in the Synura petersenii species complex (Synurophyceae, Heterokontophyta). Nova Hedwig. Beih. 136:283-98.
Laurenceau-Cornec, E. C., Trull, T. W., Davies, D. M., Christina, L. & Blain, S. 2015. Phytoplankton morphology controls on marine snow sinking velocity. Mar. Ecol. Prog. Ser. 520:35-56.
Lavau, S., Saunders, G. W. & Wetherbee, R. 1997. A phylogenetic analysis of the Synurophyceae using molecular data and scale case morphology. J. Phycol. 33:135-51.
Leadbeater, B. S. C. 1984. Silicification of cell walls of certain protistan flagellates. Phil. Trans. R. Soc. B Biol. Sci. 304:529-36.
Leadbeater, B. S. C. 1986. Scale case construction in Synura petersenii Korsch. (Chrysophyceae). In Kristiansen, J. & Andersen, R. A. [Eds.] Chrysophytes: Aspects and Problems. Cambridge University Press, Cambridge, Massachusetts, pp. 121-31.
Leadbeater, B. S. 1990. Ultrastructure and assembly of the scale case in Synura (Synurophyceae Andersen). Eur. J. Phycol. 25:117-32.
Maia, R., Rubenstein, D. R. & Shawkey, M. D. 2013. Key ornamental innovations facilitate diversification in an avian radiation. Proc. Natl. Acad. Sci. USA 110:10687-92.
Manton, I. 1955. Observations with the electron microscope on Synura caroliniana Whitford. Proc. Leeds Phil. Soc. 6:306-16.
Marron, A. O., Ratcliffe, S., Wheeler, G. L., Goldstein, R. E., King, N., Not, F., de Vargas, C. & Richter, D. J. 2016. The evolution of silicon transport in eukaryotes. Mol. Biol. Evol. 33:3226-48.
Martin-Wagenmann, B. & Gutowski, A. 1995. Scale morphology and growth characteristics of clones of Synura petersenii (Synurophyceae) at different temperatures. In Sandgren, C. D., Smol, J. P. & Kristiansen, J. [Eds.] Chrysophyte Algae: Ecology, Phylogeny and Development. Cambridge University Press, Cambridge, Massachusetts, pp. 345-60.
McGrory, C. B. & Leadbeater, B. S. C. 1981. Ultrastructure and deposition of silica in the Chrysophyceae. In Simpson, T. L. & Volcani, B. E. [Eds.] Silicon and Siliceous Structures in Biological Systems. Springer, New York, NY, pp. 201-30.
Metreveli, G., Wågberg, L., Emmoth, E., Belák, S., Strømme, M. & Mihranyan, A. 2014. A size-exclusion nanocellulose filter paper for virus removal. Adv. Healthcare Mater. 3:1546-50.
Mignot, J. P. & Brugerolle, G. 1982. Scale formation in chrysomonad flagellates. J. Ultrastruct. Res. 81:13-26.
Miller, M. A., Pfeiffer, W. & Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA. pp. 1-8.
Němcová, Y., Neustupa, J., Kvíderová, J. & Řezáčová-Škaloudová, M. 2010. Morphological plasticity of silica scales of Synura echinulata (Synurophyceae) in crossed gradients of light and temperature-a geometric morphometric approach. Nova Hedwig. Beih. 136:21-32.
Němcová, Y., Nováková, S. & Řezáčová-Škaloudová, M. 2008. Synura obesa sp. nov. (Synurophyceae) and other silica-scaled chrysophytes from Abisko (Swedish Lapland). Nova Hedwigia 86:243-54.
Němcová, Y. & Pichrtová, M. 2012. Shape dynamics of silica scales (Chrysophyceae, Stramenopiles) associated with pH. Fottea. 12:281-91.
Nicholls, K. H. & Gerrath, J. F. 1985. The taxonomy of Synura (Chrysophyceae) in Ontario with special reference to taste and odour in water supplies. Can. J. Bot. 63:1482-93.
Pančić, M. & Kiørboe, T. 2018. Phytoplankton defence mechanisms: traits and trade-offs. Biol. Rev. 93:1269-303.
Pančić, M., Torres, R. R., Almeda, R. & Kiørboe, T. 2019. Silicified cell walls as a defensive trait in diatoms. Proc. R. Soc. B Biol. Sci. 286:20190184.
Péterfi, L. S. & Momeu, L. 1977. Remarks on the taxonomy of some Synura species based on the fine structure of scales. St. Nat. 21:15-23.
Petersen, J. B. & Hansen, J. B. 1956. On the scales of some Synura species. Biol. Medd. Dan. Vid. Selsk. 23:1-38.
Pichrtová, M. & Němcová, Y. 2011. Effect of temperature on size and shape of silica scales in Synura petersenii and Mallomonas tonsurata (Stramenopiles). Hydrobiologia 673:1-11.
Pichrtová, M., Řezáčová-Škaloudová, M. & Škaloud, P. 2007. The silica-scaled chrysophytes of the Czech-Moravian Highlands. Fottea 7:43-8.
Pusztai, M., Čertnerová, D., Škaloudová, M. & Škaloud, P. 2016. Elucidating the phylogeny and taxonomic position of the genus Chrysodidymus Prowse (Chrysophyceae, Synurales). Cryptogam. Algol. 37:297-307.
Quesada-Aguilar, A., Kalisz, S. & Ashman, T. L. 2008. Flower morphology and pollinator dynamics in Solanum carolinense (Solanaceae): implications for the evolution of andromonoecy. Am. J. Bot. 95:974-84.
R Core Team 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rambaut, A. 2016. FigTree version 1.4.3. Available at: http://tree.bio.ed.ac.uk (last accessed 12 October 2020).
Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67:901.
Rasband, W. S. 1997. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA. Available at: https://imagej.nih.gov/ij/ (last accessed 12 October 2020).
Raven, J. A. 1983. The transport and function of silicon in plants. Biol. Rev. 58:179-207.
Raven, J. A. & Waite, A. M. 2004. The evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phytol. 162:45-61.
Revell, L. J. 2012. Phytools: An R package for phylogenetic comparative biology (and other things). Methods. Ecol. Evol. 3:217-23.
Řezáčová-Škaloudová, M., Neustupa, J. & Němcová, Y. 2010. Effect of temperature on the variability of silicate structures in Mallomonas kalinae and Synura curtispina (Synurophyceae). Nova Hedwig. Beih. 136:55-70.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, 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. 61:539-42.
Rubenstein, D. R. & Lovette, I. J. 2009. Reproductive skew and selection on female ornamentation in social species. Nature 462:786-9.
Sandgren, C. D., Hall, S. A. & Barlow, S. B. 1996. Siliceous scale production in chrysophyte and synurophyte algae. I. Effects of silica-limited growth on cell silica content, scale morphology, and the construction of the scale layer of Synura petersenii. J. Phycol. 32:675-92.
Saxby-Rouen, K. J., Leadbeater, B. S. C. & Reynolds, C. S. 1997. The growth response of Synura petersenii (Synurophyceae) to photon flux density, temperature, and pH. Phycologia 36:233-43.
Schnep, E. & Deichgräber, G. 1969. Über die Feinstruktur von Synura petersenii unter besonderer Berücksichtigung der Morphogenese ihrer Kieselschuppen. Protoplasma 68:85-106.
Siver, P. A. 1987. The distribution of Synura species (Chrysophyceae) in Connecticut, U.S.A. including the description of a new form. Nordic J. Bot. 7:107-16.
Siver, P. A. 2013. Synura cronbergiae sp. nov., a new species described from two Paleogene maar lakes in northern Canada. Nova Hedwigia 97:179-87.
Siver, P. A. 2015. The Synurophyceae. In Wehr, J. D., Sheath, R. G. & Kociolek, J. P. [Eds.] Freshwater Algae of North America: Ecology and Classification, 2nd edn. Academic Press, San Diego, California, USA, pp. 605-650.
Siver, P. A. & Glew, J. R. 1990. The arrangement of scales and bristles on Mallomonas (Chrysophyceae): a proposed mechanism for the formation of the cell covering. Can. J. Bot. 68:374-80.
Siver, P. A., Jo, B. Y., Kim, J. I., Shin, W., Lott, A. M. & Wolfe, A. P. 2015. Assessing the evolutionary history of the class Synurophyceae (Heterokonta) using molecular, morphometric, and paleobiological approaches. Am. J. Bot. 102:921-41.
Siver, P. A., Kapustin, D. & Gusev, E. 2018. Investigations of two-celled colonies of Synura formerly described as Chrysodidymus with descriptions of two new species. Eur. J. Phycol. 53:245-55.
Siver, P. A. & Lott, A. M. 2016. Descriptions of two new species of Synurophyceae from a bog in Newfoundland, Canada: Mallomonas baskettii sp. nov. and Synura kristiansenii sp. nov. Nova Hedwigia 102:501-11.
Siver, P. A., Lott, A. M. & Wolfe, A. P. 2013a. A summary of Synura taxa in early Cenozoic deposits from Northern Canada. Nova Hedwig. Beih. 142:181-90.
Siver, P. A. & Wolfe, A. P. 2005. Eocene scaled chrysophytes with pronounced modern affinities. Int. J. Plant Sci. 166:533-6.
Siver, P. A., Wolfe, A. P., Rohlf, F. J., Shin, W. & Jo, B. Y. 2013b. Combining geometric morphometrics, molecular phylogeny, and micropaleontology to assess evolutionary patterns in Mallomonas (Synurophyceae: Heterokontophyta). Geobiology 11:127-38.
Škaloud, P., Kristiansen, J. & Škaloudová, M. 2013. Developments in the taxonomy of silica-scaled chrysophytes-from morphological and ultrastructural to molecular approaches. Nord. J. Bot. 31:385-402.
Škaloud, P., Kynčlová, A., Benada, O., Kofroňová, O. & Škaloudová, M. 2012. Toward a revision of the genus Synura, section Petersenianae (Synurophyceae, Heterokontophyta): morphological characterization of six pseudo-cryptic species. Phycologia 51:303-29.
Škaloud, P., Škaloudová, M., Jadrná, I., Bestová, H., Pusztai, M., Kapustin, D. & Siver, P. A. 2020. Comparing morphological and molecular estimates of species diversity in the freshwater genus Synura (Stramenopiles): a model for understanding diversity of eukaryotic microorganisms. J. Phycol. 56:574-91.
Škaloud, P., Škaloudová, M., Procházková, A. & Němcová, Y. 2014. Morphological delineation and distribution patterns of four newly described species within the Synura petersenii species complex (Chrysophyceae, Stramenopiles). Eur. J. Phycol. 49:213-29.
Škaloudová, M. & Škaloud, P. 2013. A new species of Chrysosphaerella (Chrysophyceae: Chromulinales), Chrysosphaerella rotundata sp. nov., from Finland. Phytotaxa 130:34-42.
Spillane, T. 2016. Diatom frustules as a mechanical defense against predation by heterotrophic dinoflagellates. Master thesis, Western Washington University, 61 pp.
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-3.
Starmach, K. 1985. Chrysophyceae und Haptophyceae. In Ettl, H., Gerloff, J., Heynig, H. & Mollenhauer, D. [Eds.] Süsswasserflora von Mitteleuropa 1. VEB Gustav Fischer, Jena, 515 pp.
Suchard, M. A., Lemey, P., Baele, G., Ayres, D. L., Drummond, A. J. & Rambaut, A. 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4:vey016.
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. 28:2731-9.
van Tol, H. M., Irwin, A. J. & Finkel, Z. V. 2012. Macroevolutionary trends in silicoflagellate skeletal morphology: the costs and benefits of silicification. Paleobiology 38:391-402.
Walker, M. 2019. Linking shape and sinking speed in planktonic Foraminifera. PhD dissertation, University of Lincoln, UK, 292 pp.
Wee, J. L. & Andersen, R. A. 1997. Scale biogenesis in synurophycean protists: phylogenetic implications. Crit. Rev. Plant Sci. 16:497-534.
Whittall, J. B. & Hodges, S. A. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706-9.
Yoon, H. S., Hackett, J. D. & Bhattacharya, D. 2002. A single origin of the peridinin-and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. USA 99:11724-9.