Abstract
The mechanism of diatom locomotion has been widely researched but still remains a hypothesis. There are several questionable points on the prevailing model proposed by Edgar, and some of the observed phenomena cannot be completely explained by this model. In this paper, we undertook detailed investigations of cell structures, locomotion, secreted mucilage, and bending deformation for a benthic pennate diatom Navicula species. According to these broad evidences, an updated locomotion model is proposed. For Navicula sp., locomotion is realized via two or more pseudopods or stalks protruded out of the frustules. The adhesion can be produced due to the pull-off of one pseudopod or stalk from the substratum through extracellular polymeric substances. And the positive pressure is generated to balance the adhesion because of the push-down of another pseudopod or stalk onto the substratum. Because of the positive pressure, friction is generated, acting as a driving force of locomotion, and the other pseudopod or stalk can detach from the substratum, resulting in the locomotion. Furthermore, this model is validated by the force evaluation and can better explain observed phenomena. This updated model would provide a novel aspect on underwater locomotion strategy, hence can be useful in terms of artificial underwater locomotion devices.
Similar content being viewed by others
References
Arce FT, Avci R, Beech IB, Cooksey KE, Wigglesworth-Cooksey B (2004) A live bioprobe for studying diatom–surface interactions. Biophys J 87(6):4284–4297
Aumeier C, Menzel D (2012) Secretion in the diatoms. In: Vivanco JM, Baluska F (eds) Secretions and exudates in biological systems, vol 12. Springer, Heidelberg, pp 221–250
Autumn K, Liang Y, Hsieh S, Zesch W, Chan W, Kenny T, Fearing R (2000) Adhesive force of a single gecko foot-hair. Nature 405(6787):681–685
Cooksey K, Wigglesworth-Cooksey B (1995) Adhesion of bacteria and diatoms to surfaces in the sea: a review. Aquat Microb Ecol 9(1):87–96
De Stefano M, De Stefano L, Congestri R (2009) Functional morphology of micro- and nanostructures in two distinct diatom frustules. Superlattice Microst 46(1–2):64–68
Dugdale T, Dagastine R, Chiovitti A, Wetherbee R (2006a) Diatom adhesive mucilage contains distinct supramolecular assemblies of a single modular protein. Biophys J 90(8):2987–2993
Dugdale TM, Willis A, Wetherbee R (2006b) Adhesive modular proteins occur in the extracellular mucilage of the motile, pennate diatom Phaeodactylum tricornutum. Biophys J 90(8):L58–L60
Edgar L (1983) Mucilage secretions of moving diatoms. Protoplasma 118(1):44–48
Edgar L, Pickett-Heaps J (1982) Ultrastructural localization of polysaccharides in the motile diatom Navicula cuspidata. Protoplasma 113(1):10–22
Edgar L, Pickett-Heaps J (1983) The mechanism of diatom locomotion. I. An ultrastructural study of the motility apparatus. Proc R Soc London, Ser B 218(1212):331–343
Edgar L, Pickett-Heaps J (1984) Diatom locomotion. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 3. Biopress, Bristol, pp 47–88
Edgar L, Zavortink M (1983) The mechanism of diatom locomotion. II: identification of actin. Proc R Soc London, Ser B 218(1212):345–348
Geim A, Dubonos S, Grigorieva I, Novoselov K, Zhukov A, Shapoval SY (2003) Microfabricated adhesive mimicking gecko foot-hair. Nat Mater 2(7):461–463
Gordon R (1987) A retaliatory role for algal projectiles, with implications for the mechanochemistry of diatom gliding motility. J Theor Biol 126(4):419–436
Higgins M, Crawford S, Mulvaney P, Wetherbee R (2000) The topography of soft, adhesive diatom trails as observed by atomic force microscopy. Biofouling 16(2):133–139
Higgins M, Crawford S, Mulvaney P, Wetherbee R (2002) Characterization of the adhesive mucilages secreted by live diatom cells using atomic force microscopy. Protist 153(1):25–38
Higgins M, Molino P, Mulvaney P, Wetherbee R (2003) The structure and nanomechanical properties of the adhesive mucilage that mediate diatom–substratum adhesion and motility. J Phycol 39(6):1181–1193
Hoagland K, Rosowski J, Gretz M, Roemer S (1993) Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J Phycol 29(5):537–566
Huber G, Mantz H, Spolenak R, Mecke K, Jacobs K, Gorb SN, Arzt E (2005) Evidence for capillarity contributions to gecko adhesion from single spatula nanomechanical measurements. Proc Natl Acad Sci U S A 102(45):16293
Jia J, Zhou H, Gao S, Chen J (2003) A comparative investigation of the friction and wear behavior of polyimide composites under dry sliding and water-lubricated condition. Mater Sci Eng, A 356(1):48–53
Kooistra WHCF, De Stefano M, Mann DG, Salma N, Medlin LK (2003) Phylogenetic Position of Toxarium, a pennate-like lineage within the centric diatoms (Bacillariophyceae). J Phycol 39(1):185–197
Li H, Peng X, Wu L, Jia M, Zhu H (2009) Surface potential dependence of the Hamaker constant. J Phys Chem C 113(11):4419–4425
Lind J, Heimann K, Miller E, Van Vliet C, Hoogenraad N, Wetherbee R (1997) Substratum adhesion and gliding in a diatom are mediated by extracellular proteoglycans. Planta 203(2):213–221
Molino PJ, Wetherbee R (2008) The biology of biofouling diatoms and their role in the development of microbial slimes. Biofouling 24(5):365–379
Murase A, Kubota Y, Hirayama S, Kumashiro Y, Okano T, Mayama S, Umemura K (2011) Two-dimensional trajectory analysis of the diatom Navicula sp. using a micro chamber. J Microbiol Methods 87:316–319
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 & JC Lewin. J Mol Recognit 24(3):436–445
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
Schreiber U (1983) Chlorophyll fluorescence yield changes as a tool in plant physiology I. The measuring system. Photosynth Res 4(4):361–373
Silva MF, Machado JAT (2010) A survey of technologies and applications for climbing robots locomotion and adhesion. In: Miripour B (ed) Climbing and walking robots. Available from: http://www.intechopen.com/books/climbing-and-walking-robots/a-survey-of-technologies-and-applications-for-climbing-robots-locomotion-and-adhesion
Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150(1):25–32
Spangle L, Armstrong P (1973) Gliding motility of algae is unaffected by cytochalasin B. Exp Cell Res 80(2):490–493
Varenberg M, Gorb S (2008) A beetle-inspired solution for underwater adhesion. J R Soc Interface 5(20):383–385
Webster D, Cooksey K, Rubin R (1985) An investigation of the involvement of cytoskeletal structures and secretion in gliding motility of the marine diatom, Amphora coffeaeformis. Cell Motil Cytoskeleton 5(2):103–122
Wetherbee R, Lind J, Burke J, Quatrano R (1998) The first kiss: establishment and control of initial adhesion by raphid diatoms. J Phycol 34(1):9–15
Yebra D, Kiil S, Dam-Johansen K (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings. Progr Org Coating 50(2):75–104
Acknowledgment
This work was supported by the National Natural Science Foundation of China Project under grant nos. 51075228 and 51021064.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Reimer Stick
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM Video 1
(MPG 482 kb)
ESM Video 2
(MPG 614 kb)
ESM Video 3
(MPG 896 kb)
Rights and permissions
About this article
Cite this article
Wang, J., Cao, S., Du, C. et al. Underwater locomotion strategy by a benthic pennate diatom Navicula sp.. Protoplasma 250, 1203–1212 (2013). https://doi.org/10.1007/s00709-013-0502-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-013-0502-2