Abstract
Diatoms stand out among other microalgae due to the high diversity of species-specific silica frustules whose components (valves and girdle bands) are formed within the cell in special organelles called silica deposition vesicles (SDVs). Research on cell structure and morphogenesis of frustule elements in diatoms of different taxonomic groups has been carried out since the 1950s but is still relevant today. Here, cytological features and valve morphogenesis in the freshwater raphid pennate diatom Encyonema ventricosum (Agardh) Grunow have been studied using light and transmission electron microscopy of cleaned frustules and ultrathin sections of cells, and scanning electron and atomic force microscopy of the frustule surface. Data have been obtained on chloroplast structure: the pyrenoid is spherical, penetrated by a lamella (a stack of two thylakoids); the girdle lamella consists of several short lamellae. The basic stages of frustule morphogenesis characteristic of raphid pennate diatoms have been traced, with the presence of cytoskeletal elements near SDVs being observed throughout this process. Degradation of the plasmalemma and silicalemma is shown to take place when the newly formed valve is released into the space between sister cells. The role of vesicular transport and exocytosis in the gliding of pennate diatoms is discussed.
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References
Bedoshvili Y, Popkova T, Likhoshway Y (2009) Chloroplast structure of diatoms of different classes. Cell Tissue Biol 3:297–310. https://doi.org/10.1134/S1990519X09030122
Bedoshvili Y, Kaluzhnaya O, Likhoshway Y (2012) The frustule morphogenesis of Aulacoseira baicalensis in the natural population. J Adv Microsc Res 7:218–224. https://doi.org/10.1166/jamr.2012.1119
Chiappino ML, Volcani BE (1977) Studies on the biochemistry and fine structure of silica shell formation in diatoms VII. Sequential cell wall development in the pennate Navicula pelliculosa. Protoplasma 93(2-3):205–221. https://doi.org/10.1007/BF01275654
Crawford S, Higgins M, Mulvaney P, Wetherbee R (2001) Nanostructure of the diatom frustule as revealed by atomic force and scanning electron microscopy. J Phycol 37(4):543–554. https://doi.org/10.1046/j.1529-8817.2001.037004543.x
Crawford R (1981) The siliceous components of the diatom cell wall and their morphological variation. In: Simpson TL, Volcani BE (eds) Silicon and siliceous structures in biological systems. Springer-Verlag, New York, pp 129–156. https://doi.org/10.1007/978-1-4612-5944-2_6
Crawford R, Schmid AM (1986) Ultrastructure of silica deposition in diatoms. In: Leadbeater BS and Riding R (eds) Biomineralization in lower plants and animals. The Systematics Association Special, vol 30. Oxford University Press, Oxford, pp 291–314
Dawson PA (1973) Observation on the structure of some forms of Gomphonema parvulum Kütz. III. Frustule formation. J Phycol 9:353–365
Drum RW, Pankratz HS (1964) Post mitotic fine structure of Gomphonema parvulum. J Ultrastruct Res 10(3-4):217–223. https://doi.org/10.1016/S0022-5320(64)80006-X
Edgar LA, Pickett-Heaps JD (1983) The mechanism of diatom locomotion. I. An ultrastructural study of the motility apparatus. Proc R Soc Lond 218(1212):331–343. https://doi.org/10.1098/rspb.1983.0042
Ehrlich H, Witkowski A (2015) Biomineralization in diatoms: the organic templates. Biol Inspir Syst 6:39–58. https://doi.org/10.1007/978-94-017-9398-8_3
Flori S, Jouneau PH, Finazzi G, Marechal E, Falconet D (2016) Ultrastructure of the periplastidial compartment of the diatom Phaeodactylum tricornutum. Protist 167(3):254–267. https://doi.org/10.1016/j.protis.2016.04.001
Geitler L (1959) Morphologische, entwicklungsgcshichtliehe und systematische Notizen über einige Süsswasseralgen. Österr Bot Z 106(1-2):159–171. https://doi.org/10.1007/BF01279004
Geitler L (1981) Die Lage des Chromatophors in Beziehung zur Systematik von Cymbella-Arten (Bacillariophyceae). Pl Syst Evol 138(1-2):153–156. https://doi.org/10.1007/BF00984616
Grachev M, Annenkov V, Likhoshway Y (2008) Silicon nanotechnologies of pigmented heterokonts. BioEssays 30(4):328–337. https://doi.org/10.1002/bies.20731
Hammer JA, Sellers JR (2012) Walking to work: roles for class V myosins as cargo transporters. Nat Rev Mol Cell Biol 13:13–26
Higgins MJ, Molino P, Mulvaney P, Wetherbee R (2003) The structure and nanomechanical properties of the adhesive mucilage that mediates diatom-substratum adhesion and motility. J Phycol 39(6):1181–1193. https://doi.org/10.1111/j.0022-3646.2003.03-027.x
Hildebrand M, Wetherbee R (2003) Components and control of silicification in diatoms. In: Muller WEG (ed) Silicon biomineralization. Biology, biochemistry, molecular biology, biotechnology (Progress in molecular and subcellular biology, Vol. 33). Springer-Verlag, New-York, pp 11–58
Kharitonenko K, Bedoshvili Y, Likhoshway Y (2015) Changes in the micro- and nanostructure of siliceous frustule valves in the diatom Synedra acus under the effect of colchicine treatment at different stages of the cell cycle. J Struct Biol 190(1):73–80. https://doi.org/10.1016/j.jsb.2014.12.004
Kociolek JP, Sicko-Goad L, Stoermer EF (1990) Cytoplasmic fine structure of two Encyonema species. In: Kociolek P (Ed.) Proceedings of the 11th International Diatom Symposium. San-Francisco, California Academy of Sciences. pp 235–245
Li CW, Volcani B (1984) Aspects of silicification in wall morphogenesis of diatoms. Phil Trans Roy Soc London B 304(1121):519–528. https://doi.org/10.1098/rstb.1984.0043
Lodish H, Berk A, Kaiser C, Krieger M, Scott M, Bretcher A, Ploegh H, Matsudaira P (2007) Molecular cell biology. WH Freeman and Company, New York
Mann DG (1984) An ontogenetic approach to diatom systematics. In: Mann DG (ed) Proceedings of the seventh international diatom symposium. O Koeltz, Koenigstein, pp 113–144
Medlin LK, Kaczmarska I (2004) Evolution of the diatoms: V. Morphological and cytological support of the major clades and taxonomic revision. Phycologia 43(3):245–227. https://doi.org/10.2216/i0031-8884-43-3-245.1
Parkinson J, Brechet Y, Gordon R (1999) Centric diatom morphogenesis: a model based on a DLA algorithm investigating the potential role of microtubules. Biochim Biophys Acta 1452(1):89–102. https://doi.org/10.1016/S0167-4889(99)00116-0
Pickett-Heaps JD (1998) Cell division and morphogenesis of the centric diatom Chaetoceros decipiens (Bacillariophiceae) II. Electron microscopy and a new paradigm for tip growth. J Phycol 34(6):995–1004. https://doi.org/10.1046/j.1529-8817.1998.340995.x
Pickett-Heaps JD, Schmid AM, Edgar L (1990) The cell biology of diatom wall morphogenesis. Progress in phycological research. Biopress Ltd, Bristol
Poulsen N, Spector I, Spurck T, Schultz T, Wetherbee R (1999) Diatom gliding is the result of an actin–myosin motility system. Cell Motil Cytoskeleton 44(1):23–33. https://doi.org/10.1002/(SICI)1097-0169(199909)44:1<23::AID-CM2>3.0.CO;2-D
Reimann BEF (1964) Deposition of silica inside a diatom cell. Exp Cell Res 34(3):605–608. https://doi.org/10.1016/0014-4827(64)90248-4
Reimann B, Lewin J, Volcani B (1966) Studies on the biochemistry and fine structure of silica shell formation in diatoms. II. The structure of the cell wall of Navicula pelliculosa (Breb.) Hilse. J Phycol 2(2):74–84. https://doi.org/10.1111/j.1529-8817.1966.tb04597.x
Round FE, Crawford RM, Mann DG (1990) The diatoms. Cambridge University Press, Bristol
Schmid AM, Schultz D (1979) Wall morphogenesis in diatoms: deposition of silica by cytoplasmic vesicles. Protoplasma 100(3-4):267–288. https://doi.org/10.1007/BF01279316
Schmid AM (2001) Value of pyrenoids in the systematics of the diatoms: their morphology and ultrastructure. In Economou-Amilli A (Ed) Proceedings of the 16th international diatom symposium. Amvrosiou press, Athens, pp 1–32
Schnepf E, Deichgraber G, Drebes G (1980) Morphogenetic processes in Attheya decora (Bacillariophyceae, Biddulphiineae). Pl Syst Evol 135(3-4):265–277. https://doi.org/10.1007/BF00983191
Stoermer E, Pankratz H, Bowen C (1965) Fine structure of the diatom Amphipleura pellucida. II. Cytoplasmic fine structure and frustule formation. Am J Bot 52(10):1067–1078. https://doi.org/10.2307/2440138
Sullivan CW (1979) Diatom mineralization of silicic acid. IV. Kinetics of soluble Si pool formation in exponentially growing and synchronized Navicula pelliculosa. J Phycol 15(2):210–216. https://doi.org/10.1111/j.0022-3646.1979.00210.x
Sumper M, Kröger N (2004) Silica formation in diatoms: the function of long-chain polyamines and silaffins. J Mater Chem 14(14):2059–2065. https://doi.org/10.1039/B401028K
Tanaka A, De Martino A, Amato A, Montsant A, Mathieu B, Rostang P, Tirichine L, Bowler C (2015) Ultrastructure and membrane traffic during cell division in the marine pennate diatom Phaeodactylum tricornutum. Protist 166(5):506–521. https://doi.org/10.1016/j.protis.2015.07.005
Tesson B, Hildebrand M (2010) Extensive and intimate association of the cytoskeleton with forming silica in diatoms: control over patterning on the meso- and micro-scale. PLoS One 5(12):e14300. https://doi.org/10.1371/journal.pone.0014300
Thompson AS, Rhodes JC, Pettman I (1988) Culture collection of algae and protozoa: catalogue of strains. Kendal,Titus Wilson and Son, Cumbria
Van de Meene AML, Pickett-Heaps JD (2002) Valve morphogenesis in the centric diatom Proboscia alata Sundström. J Phycol 38(2):351–363. https://doi.org/10.1046/j.1529-8817.2002.01124.x
Von Stosch HA (1981) Structural and histochemical observations on the organic layers of the diatom cell wall. In: Ross R (Ed) Proceedings of 6th symposium on recent and fossil diatoms. Koeltz, Koenigstein, pp 231–252
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This study was supported by the Federal Agency for Scientific Organizations, project no. 0345-2016-0001.
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Bedoshvili, Y.D., Gneusheva, K.V., Popova, M.S. et al. Frustule morphogenesis of raphid pennate diatom Encyonema ventricosum (Agardh) Grunow. Protoplasma 255, 911–921 (2018). https://doi.org/10.1007/s00709-017-1199-4
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DOI: https://doi.org/10.1007/s00709-017-1199-4