The Molecular Basis of Diatom Adhesion and Motility
Cell Biology
Final Report Abstract
Diatoms are a diverse group of unicellular eukaryotic algae with intricately patterned silica cell walls and their major role in global ecosystems, contributing ~20% of global carbon fixation. Benthic, pennate diatoms are well known for their adhesion strength to natural and man-made surfaces forming dense brown biofilms on submerged surfaces. So far, the molecular mechanisms of adhesion and gliding motility of pennate diatoms have remained largely unknown. This project aimed to unravel these mechanisms by identifying both extracellular adhesive proteins and intracellular components that link the actin–myosin cytoskeleton to the adhesive proteins. Using a combination of proteomics, molecular genetics, and live-cell imaging, we focused on Craspedostauros australis and Amphora coffeaeformis as models for benthic, pennate diatoms. Proteomic analysis led to the discovery of the first proteins in purified adhesive trail material. To date, around 30 candidate adhesive proteins have been identified. Phylogenetic analysis revealed that many of these proteins are specific to pennate diatoms, and immunofluorescence localization confirmed that seven of these are structural components of the adhesive trails. Notably, the Choice-of-Anchor A (CAA) domain, which has been acquired from bacteria through horizontal gene transfer, is a widespread domain in the adhesive trail proteins. Structural modelling of the CAA domain revealed similarities with ice-binding proteins, suggesting a potential role in mediating protein–surface interactions and leading to ongoing experimental studies. To investigate the molecular foundations of diatom gliding, we used phylogenetic analysis to identify raphid-specific myosins. Through GFP-tagging and time-lapse microscopy we show a direct correlation between the intracellular movement of the GFP-tagged myosins and the gliding motility of the cell. To monitor the dynamics of adhesive secretion during movement, we developed a lectin-based live-cell imaging tool that allowed visualization of adhesive material deposition in real time and revealed a quantitative correlation between secretion activity and gliding speed. Our results from a proteomics study identified further candidate components of the diatom adhesion motility complex. Altogether, our work provides a molecular basis for understanding the mechanisms of diatom adhesion and motility, opening new avenues for developing bio-inspired adhesives, antifouling strategies, and sustainable materials production.
Publications
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Identification of proteins in the adhesive trails of the diatom Amphora coffeaeformis. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1784), 20190196.
Lachnit, Martina; Buhmann, Matthias T.; Klemm, Jennifer; Kröger, Nils & Poulsen, Nicole
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Mating type specific transcriptomic response to sex inducing pheromone in the pennate diatom Seminavis robusta. The ISME Journal, 15(2), 562-576.
Bilcke, Gust; Van den Berge, Koen; De Decker, Sam; Bonneure, Eli; Poulsen, Nicole; Bulankova, Petra; Osuna-Cruz, Cristina Maria; Dickenson, Jack; Sabbe, Koen; Pohnert, Georg; Vandepoele, Klaas; Mangelinckx, Sven; Clement, Lieven; De Veylder, Lieven & Vyverman, Wim
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The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms. Nature Communications, 11(1).
Osuna-Cruz, Cristina Maria; Bilcke, Gust; Vancaester, Emmelien; De Decker, Sam; Bones, Atle M.; Winge, Per; Poulsen, Nicole; Bulankova, Petra; Verhelst, Bram; Audoor, Sien; Belisova, Darja; Pargana, Aikaterini; Russo, Monia; Stock, Frederike; Cirri, Emilio; Brembu, Tore; Pohnert, Georg; Piganeau, Gwenael; Ferrante, Maria Immacolata ... & Vandepoele, Klaas
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Diurnal transcript profiling of the diatom Seminavis robusta reveals adaptations to a benthic lifestyle. The Plant Journal, 107(1), 315-336.
Bilcke, Gust; Osuna‐Cruz, Cristina Maria; Santana Silva, Marta; Poulsen, Nicole; D.’hondt, Sofie; Bulankova, Petra; Vyverman, Wim; De Veylder, Lieven & Vandepoele, Klaas
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Diatom Adhesion and Motility. The Molecular Life of Diatoms, 367-393. Springer International Publishing.
Poulsen, Nicole; Davutoglu, Metin Gabriel & Zackova Suchanova, Jirina
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On the role of cell surface associated, mucin‐like glycoproteins in the pennate diatom Craspedostauros australis (Bacillariophyceae). Journal of Phycology, 59(1), 54-69.
Poulsen, Nicole; Hennig, Helene; Geyer, Veikko F.; Diez, Stefan; Wetherbee, Richard; Fitz‐Gibbon, Sorel; Pellegrini, Matteo & Kröger, Nils
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Diatom adhesive trail proteins acquired by horizontal gene transfer from bacteria serve as primers for marine biofilm formation. New Phytologist, 240(2), 770-783.
Zackova Suchanova, Jirina; Bilcke, Gust; Romanowska, Beata; Fatlawi, Ali; Pippel, Martin; Skeffington, Alastair; Schroeder, Michael; Vyverman, Wim; Vandepoele, Klaas; Kröger, Nils & Poulsen, Nicole
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Gliding motility of the diatom Craspedostauros australis coincides with the intracellular movement of raphid-specific myosins. Communications Biology, 7(1).
Davutoglu, Metin G.; Geyer, Veikko F.; Niese, Lukas; Soltwedel, Johannes R.; Zoccoler, Marcelo L.; Sabatino, Valeria; Haase, Robert; Kröger, Nils; Diez, Stefan & Poulsen, Nicole
