Motility modes of Spiroplasma melliferum BC3: A helical, wall-less bacterium driven by a linear motor

Abstract

Spiroplasma are members of the Mollicutes (Mycoplasma, Acholeplasma and Spiroplasma) - the simplest, minimal, free-living and self-replicating forms of life. The mollicutes are unique among bacteria in completely lacking cell walls and flagella and in having an internal, contractile cytoskeleton, which also functions as a linear motor. Spiroplasma are helical, chemotactic and viscotactic active swimmers. The Spiroplasmal cytoskeleton is a flat ribbon composed of seven pairs of fibrils. The ribbon is attached to the inner side of the cell membrane along its innermost (shortest) helical line. The cell's geometry and dynamic helical parameters, and consequently motility, can be controlled by changing differentially and in a co-ordinated manner, the length of the fibrils. We identified several consistent modes of cell movements and motility originating, most likely, as a result of co-operative or local molecular switching of fibrils: (i) regular extension and contraction within the limits of helical symmetry (this mode also includes straightening, beyond what is allowed by helical symmetry, and reversible change of helical sense); (ii) spontaneous and random change of helical sense originating at random sites along the cell (these changes propagate along the cell in either direction and hand switching is completed within ∼0.08 second); (iii) forming a deformation on one of the helical turns and propagating it along the cell (these helical deformations may travel along the cell at a speed of up to ∼40 μm s-1); (iv) random bending, flexing and twitching (equivalent to tumbling). In standard medium (viscosity= 1.147 centipoise) the cells run at ∼1.5 μm s-1, have a Reynolds number of ∼3.5 × 10-6 and consume ∼30 ATP molecules s-1. Running velocity, duration, persistence and efficiency increase with viscosity upon adding ficoll, dextran and methylcellulose to standard media. Relative force measurements using optical tweezers confirm these findings.