The cell distributes energy between two main branches: locomotion, and reproduction. This partitioning scheme is dynamic, and dependent on the cell's environment. In view of deconvoluting this energy balance, we present an investigation of the costs associated with cellular locomotion in Bacteroidetes. This exemplary organism displays a unique gliding motility. Such translocation is independent of well-known propulsive structures like flagella, pili, or fimbriae; rather, the cell uniquely glides on a surface. I will present a ‘rotary rack and pinion’ model engaging the Type IX Secretion System rotary motor to describe the gliding mechanism. (1) Using a Bayesian model of maximum entropy, we investigate the torque-guided, conformational landscape of the Secretion System in the periplasmic space. After 2 microseconds of simulation, an allosteric network is discovered that couples the power-strokes in the peripheral domains with the rotatory proton-pumping in the transmembrane part of the motor. (2) In analogy with our past computations of rotary ATPases, a combination of pH-simulations and Anisotropic Network Model are separately employed to decipher the chemo-mechanical forces that drive proton gradient across the motor. These coupling forces are monitored using light microscopy and tuned biochemically using mutations to control the gliding movements of the bacteria. (3) Finally, guided by recent cryo-EM experiments, both the periplasmic and membrane domains of the secretion system are integrated to drive a kinetic description of the energy cost associated with gliding motility, comparing with the growth necessities.