Nanoscale Visualization of a Fibrillar Array in the Cell Wall of Filamentous Cyanobacteria and Its Implications for Gliding Motility

Abstract

Many filamentous cyanobacteria are motile by gliding, which requires attachment to a surface. There are two main theories to explain the mechanism of gliding. According to the first, the filament is pushed forward by small waves that pass along the cell surface. In the second, gliding is powered by the extrusion of slime through pores surrounding each cell septum. We have previously shown that the cell walls of several motile cyanobacteria possess an array of parallel fibrils between the peptidoglycan and the outer membrane and have speculated that the function of this array may be to generate surface waves to power gliding. Here, we report on a study of the cell surface topography of two morphologically different filamentous cyanobacteria, using field emission gun scanning electron microscopy (FEGSEM) and atomic force microscopy (AFM). FEGSEM and AFM images of Oscillatoria sp. strain A2 confirmed the presence of an array of fibrils, visible as parallel corrugations on the cell surface. These corrugations were also visualized by AFM scanning of fully hydrated filaments under liquid; this has not been achieved before for filamentous bacteria. FEGSEM images of Nostoc punctiforme revealed a highly convoluted, not parallel, fibrillar array. We conclude that an array of parallel fibrils, beneath the outer membrane of Oscillatoria, may function in the generation of thrust in gliding motility. The array of convoluted fibrils in N. punctiforme may have an alternative function, perhaps connected with the increase in outer membrane surface area resulting from the presence of the fibrils.Cyanobacteria are phototrophic prokaryotes that vary in morphology from unicellular strains to filamentous forms capable of complex cellular differentiation (1, 2). Many cyanobacteria are motile. Some unicellular Synechococcus strains are capable of swimming by a mechanism that does not employ flagella (28) in which thrust is generated by an extracellular protein, SwmA (6, 19), but most motile cyanobacteria employ gliding, which requires attachment to a surface. The unicellular Synechocystis sp. strain PCC 6803 moves by a form of gliding often referred to as twitching motility, which is powered by type IV pili on the cell surface (4,5,30). In filamentous strains, in which forward movement is often accompanied by rotation of the filament about its long axis (10), the mechanism of gliding is unknown. Halfen and Castenholz proposed a model for gliding (11) based on the results of their own electron microscopy (EM) studies of motile filamentous cyanobacteria and on the theories of Jarosch (16). They speculated that the motor for gliding in the filamentous Oscillatoriaceae might be provided by proteinaceous contractile fibrils, 6 to 9 nm in diameter, located between the peptidoglycan layer and the outer membrane (OM) and that rotation of the filaments during gliding might be a result of the helical arrangement of the fibrils. An ultrastructural examination of the cell walls of four gliding filamentous cyanobacteria by Hoiczyk and Baumeister (12...

Evidence that a modified type IV pilus‐like system powers gliding motility and polysaccharide secretion in filamentous cyanobacteria

“…A second theory postulates that contraction waves driven by contractile fibers provide the motive force. Evidence in support of this theory is limited to a handful of conflicting ultrastructure studies that found various fibrils either internal or external to the outer membrane in several strains of filamentous cyanobacteria (Halfen and Castenholz, 1970;Hoiczyk and Baumeister, 1995;Adams et al, 1998;Read et al, 2007). The third theory holds that like Synechocystis, T4P provide the motive force.…”

Chemical and mechanical signals in inducingPhormidium(Cyanobacteria) defence against their grazers

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