Abstract
Atomic force microscopy (AFM) allows high image resolution, based on slight differences in surface height and on imaging transparent structures, thus, is an excellent type of microscopy for imaging nano-sized objects, such as diatoms. Currently and since 1992, the number of publications applying AFM on diatom studies has increased significantly. Our study considers different aspects related with AFM and diatom samples preparation, AFM types and its application in studies of taxonomy, biomineral formation, ultrastructure, mucilage layers, and micromechanical properties. We also present new AFM data highlighting the taxonomical importance of Amphipleura pellucida. From our knowledge, it is the first general review that compiles all the works carried out on Atomic force microscopy (AFM) applied to diatoms, highlighting the AFM advantages regarding the study of these microorganisms as a whole.
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References
Almqvist N, Delamo Y, Smith BL, Thomson NH, Bartholdson Å, Lal R, Brzezinski M, Hansma PK (2001) Micromechanical and structural properties of a pennate diatom investigated by atomic force microscopy. J Microsc 202:518–532
Arce FT, Avci R, Beech IB, Cooksey KE, Wigglesworth-Cooksey B (2004) A live bioprobe for studying diatom-surface interactions. Biophys J 87:4284–4297
Balnois E, Wilkinson KJ (2002) Sample preparation techniques for the observation of environmental biopolymers by atomic force microscopy. Colloids Surf A Physicochem Eng Asp 207:229–242
Binnig G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56:930–933
Borowitzka MA, Volcani BE (1978) The polymorphic diatom Phaeodactylum tricornutum: ultrastructure of its morphotypes. J Phycol 14:10–21
Bosak S, Pletikapić G, Hozić A, Svetličić V, Sarno D, Viličić D (2012) A novel type of colony formation in marine planktonic diatoms revealed by atomic force microscopy. PLoS One 7:e44851
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 93:205–221
Chiovitti A, Higgins MJ, Harper RE, Wetherbee R, Bacic A (2003) The complex polysaccharides of the raphid diatom Pinnularia viridis (Bacillariophyceae). J Phycol 39:543–554
Chiovitti A, Harper RE, Willis A, Bacic A, Mulvaney P, Wetherbee R (2005) Variations in the substituted 3-linked mannans closely associated with the silicified walls of diatoms. J Phycol 41:1154–1161
Clarson SJ, Steinitz-Kannan M, Patwardhan SV, Kannan R, Hartig R, Schloesser L, Hamilton DW, Fusaro JKA, Beltz R (2009) Some observations of diatoms under turbulence. SILICON 1:79–90
Crawford SA, Higgins MJ, Mulvaney P, Wetherbee R (2001) Nanostructure of the diatom frustule as revealed by atomic force and scanning electron microscopy. J Phycol 37:543–554
De Stefano L, De Stefano M, De Tommasi E, Rea I, Rendina I (2011) A natural source of porous biosilica for nanotech applications: the diatoms microalgae. Phys Status Solidi C 8:1820–1825
Drake B, Prater CB, Weisenhorn AL, Gould SAC, Albrecht TR, Quate CF, Cannel DS, Hansma HG, Hansma PK (1989) Imaging crystals, polymers, and processes in water with the atomic force microscope. Science 243:1586–1589
Dugdale TM, Dagastine R, Chiovitti A, Mulvaney P, Wetherbee R (2005) Single adhesive nanofibers from a live diatom have the signature fingerprint of modular proteins. Biophys J 89:4252–4260
Engel A, Gaub HE (2008) Structure and mechanics of membrane proteins. Annu Rev Biochem 77:127–148
Ford CW, Percival E (1965) The carbohydrates of Phaeodactylum tricornutum. Part I. Preliminary examination of the organism, and characterisation of low molecular weight material and of a glucan. J Chem Soc 1298:7035–7041
Francius G, Tesson B, Dague E, Martin-Jézéquel V, Dufrêne YF (2008) Nanostructure and nanomechanics of live Phaeodactylum tricornutum morphotypes. Environ Microbiol 10:1344–1356
Francois JM, Formosa C, Schiavone M, Pillet F, Martin-Yken H, Dague E (2013) Use of atomic force microscopy (AFM) to explore cell wall properties and response to stress in the yeast Saccharomyces cerevisiae. Curr Genet 59:187–196
Gebeshuber IC, Thompson JB, Del Amo Y, Stachelberger H, Kindt JH (2002) In vivo nanoscale atomic force microscopy investigation of diatom adhesion properties. Mater Sci Technol 18:763–766
Gebeshuber IC, Kindt JH, Thompson JB, Del Amo Y, Stachelber H, Brzezinski MA, Stucky GD, Morse DE, Hansma PK (2003) Atomic force microscopy study of living diatoms in ambient conditions. J Microsc 212:292–299
Gebeshuber IC, Stachelberger H, Drack M (2005) Diatom bionanotribology—biological surfaces in relative motion: their design, friction, adhesion, lubrication and wear. J Nanosci Nanotechnol 5:79–87
Harper MA, Harper JF (1967) Measurements of diatom adhesion and their relationship with movement. Br Phycol Bull 3:195–207
Heredia A, Silva S, Santos C, Delgadillo I, Vrieling EG (2008) Analysis of cross-sections of Ditylum brightwelli biosilica by tap** mode atomic force microscopy and scanning electron microscopy. J Scann Probe Microsc 3:19–24
Higgins MJ, Crawford SA, Mulvaney P, Wetherbee R (2000) The topography of soft, adhesive diatom ‘trails’ as observed by atomic force microscopy. Biofouling 16:133–139
Higgins MJ, Crawford SA, Mulvaney P, Wetherbee R (2002) Characterization of the adhesive mucilages secreted by live diatom cells using atomic force microscopy. Protist 153:25–38
Higgins MJ, Sader JE, Mulvaney P, Wetherbee R (2003a) Probing the surface of living diatoms with atomic force microscopy: the nanostructure and nanomechanical properties of the mucilage layer. J Phycol 39:722–734
Higgins MJ, Molino P, Mulvaney P, Wetherbee R (2003b) The structure and nanomechanical properties of the adhesive mucilage that mediates diatom-substratum adhesion and motility. J Phycol 39:1181–1193
Hildebrand M, York E, Kelz JI, Davis AK, Frigeri LG, Allison DP, Doktycz MJ (2006) Nanoscale control of silica morphology and three-dimensional structure during diatom cell wall formation. J Mater Res 21:2689–2698
Hildebrand M, Frigeri LG, Davis AK (2007) Synchronized growth of Thalassiosira pseudonana (Bacillariophyceae) provides novel insights into cell-wall synthesis processes in relation to the cell cycle. J Phycol 43:730–740
Hildebrand M, Doktycz MJ, Allison DP (2008) Application of AFM in understanding biomineral formation in diatoms. Pflugers Arch Eur J Physiol 456:127–137
Hildebrand M, Holton G, Joy DC, Doktycz MJ, Allison DP (2009) Diverse and conserved nano- and mesoscale structures of diatom silica revealed by atomic force microscopy. J Microsc 235:172–187
Hlúbiková D, Luís AT, Vaché V, Ector L, Hoffmann L, Choquet P (2012) Optimization of the replica molding process of PDMS using pennate diatoms. J Micromech Microeng 22:115019
Karp-Boss L, Gueta R, Rousso I (2014) Judging diatoms by their cover: variability in local elasticity of Lithodesmium undulatum undergoing cell division. PLoS One 9:e109089
Kolbe R, Golz E (1943) Elektronenoptische Diatomeen Studien. Ber Deutsch Bot Ges 61:91–98
Kröger N, Lorenz S, Brunner E, Sumper M (2002) Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298:584–586
Lewin JC (1955) The capsule of the diatom Navicula pelliculosa. J Gen Microbiol 13:162–169
Lewin JC, Lewin RA, Philpott DE (1958) Observations on Phaeodactylum tricornutum. J Gen Microbiol 18:418–426
Linder A, Colchero J, Apell HJ, Marti O, Mlynek J (1992) Scanning force microscopy of diatom shells. Ultramicroscopy 42–44:329–332
Losic D, Mitchell JG, Voelcker NH (2006a) Fabrication of gold nanostructures by templating from porous diatom frustules. New J Chem 30:908–914
Losic D, Rosengarten G, Mitchell JG, Voelcker NH (2006b) Pore architecture of diatom frustules: potential nanostructured membranes for molecular and particle separations. J Nanosci Nanotech 6:982–989
Losic D, Pillar RJ, Dilger T, Mitchell JG, Voelcker NH (2007a) Atomic force microscopy (AFM) characterisation of the porous silica nanostructure of two centric diatoms. J Porous Mater 14:61–69
Losic D, Short K, Mitchell JG, Lal R, Voelcker NH (2007b) AFM nanoindentations of diatom biosilica surfaces. Langmuir 23:5014–5021
Losic D, Mitchell JG, Voelcker NH (2008) Diatom culture media contain extracellular silica nanoparticles which form opalescent films. In: Voelcker NH, Thissen HW (eds) Smart Materials V. Proc. SPIE 7267:726712
Lowenstam HA, Epstein S (1957) On the origin of sedimentary aragonite needles of the great Bahama Bank. J Geol 65:364–375
Noll F, Sumper M, Hampp N (2002) Nanostructure of diatom silica surfaces and of biomimetic analogues. Nano Lett 2:91–95
Pickett-Heaps J, Schmid AMM, Edgar LA (1990) The cell biology of diatom valve formation. Prog Phycol Res 7:1–168
Pletikapić G, Radić TM, Zimmermann AH, Svetličić V, Pfannkuchen M, Marić D, Godrijan J, Žutić V (2011) AFM imaging of extracellular polymer release by marine diatom Cylindrotheca closterium (Ehrenberg) Reiman & J.C. Lewin. J Mol Recognit 24:436–445
Pletikapić G, Berquand A, Radić TM, Svetličić V (2012) Quantitative nanomechanical map** of marine diatom in seawater using peak force tap** atomic force microscopy. J Phycol 48:174–185
Rief M, Oesterhelt F, Heymann B, Gaub HE (1997) Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 275:1295–1297
Round FE, Crawford RM, Mann DG (1990) The diatoms: Biology & morphology of the genera. Cambridge University Press, Cambridge
Rugar D, Hansma P (1990) Atomic force microscopy. Phys Today 43:23–30
Scheffel A, Poulsen N, Shian S, Kröger N (2011) Nanopatterned protein microrings from a diatom that direct silica morphogenesis. Proc Natl Acad Sci U S A 108:3175–3180
Smith BL, Schäffer TE, Viani M, Thompson JB, Frederick NA, Kindt J, Belcher A, Stucky GD, Morse DE, Hansma PK (1999) Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399:761–763
Stal LJ, de Brouwer JFC (2003) Biofilm formation by benthic diatoms and their influence on the stabilization of intertidal mudflats. Ber Forschungszentrum Terramare 12:109–111
Strzelecki J, Dąbrowski M, Strzelecka J, Tszydel M, Mikulska K, Nowak W, Balter A (2012) AFM investigation of biological nanostructures. Acta Phys Pol A 122:329–332
Sumper M, Kröger N (2004) Silica formation in diatoms: the function of long-chain polyamines and silaffins. J Mater Chem 14:2059–2065
Svetličić V, Žutić V, Radić TM, Pletikapić G, Zimmermann AH, Urbani R (2011) Polymer networks produced by marine diatoms in the northern Adriatic Sea. Mar Drugs 9:666–679
Svetličić V, Žutić V, Pletikapić G, Radić TM (2013) Marine polysaccharide networks and diatoms at the nanometric scale. Int J Mol Sci 14:20064–20078
Tesson B, Hildebrand M (2010) Dynamics of silica cell wall morphogenesis in the diatom Cyclotella cryptica: substructure formation and the role of microfilaments. J Struct Biol 169:62–74
Tesson B, Hildebrand M (2013) Characterization and localization of insoluble organic matrices associated with diatom cell walls: insight into their roles during cell wall formation. PLoS One 8:e61675
Tokuda H (1969) Excretion of carbohydrate by a marine pennate diatom, Nitzschia closterium. Rec Oceanogr Works Jpn 10:109–122
Villacorte LO, Ekowati Y, Neu TR, Kleijn JM, Winters H, Amy G, Schippers JC, Kennedy MD (2015) Characterisation of algal organic matter produced by bloom-forming marine and freshwater algae. Water Res 73:216–230
Wang Y, Zhang D, Cai J, Pan J, Chen M, Li A, Jiang Y (2012) Biosilica structures obtained from Nitzschia, Ditylum, Skeletonema, and Coscinodiscus diatom by a filtration-aided acid cleaning method. Appl Microbiol Biotechnol 95:1165–1178
Weyn B, Kalle W, Kumar-Singh S, Van Marck E, Tanke H, Jacob W (1998) Atomic force microscopy: influence of air drying and fixation on the morphology and viscoelasticity of cultured cells. J Microsc 189:172–180
Acknowledgements
This work was carried out in the framework of the project REVAD (C08/MS/10) supported by the National Research Fund of Luxembourg. We are grateful to Dr. Diba Khan-Bureau, Professor & Program Coordinator of Environmental Engineering Technology & Biology TAP CSCU Pathways from Three Rivers Community College (Norwich, Connecticut, USA) for revising the English.
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Luís, A.T., Hlúbiková, D., Vaché, V. et al. Atomic force microscopy (AFM) application to diatom study: review and perspectives. J Appl Phycol 29, 2989–3001 (2017). https://doi.org/10.1007/s10811-017-1177-4
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DOI: https://doi.org/10.1007/s10811-017-1177-4