Microbial communities are key engines that drive earth’s biogeochemical cycles. However, ecosystem models today exhibit only limited abilities in predicting microbial dynamics and require the calibration of multiple population specific empirical equations. In contrast, we build on a new kinetic "Microbial Transition State" (MTS) theory of growth derived from first physical principles. We show how the theory coupled to simple mass and energy balance calculations constitutes a framework that intrinsically enclose important qualitative properties to model microbial community dynamics. We first show how the theory can take into account simultaneously the influence of all resources needed for growth (electron donor, acceptor and nutrients) while still producing consistent dynamics fulfilling the Liebig rule of the single limiting substrate. We also show the apparition of consistent energy-dependent microbial successions in mixed culture settings without the need for population-specific parameter calibration. Then, we illustrate how this approach can be used to model a simplified activated sludge community. For that, we compare MTS-derived dynamics to these of a widely used activated sludge model and show that similar growth yields and overall dynamics can be obtained using 2 parameters instead of 12. This new kinetic theory of growth grounded by a set of generic physical principles thus parsimoniously give rise to consistent microbial population and community dynamics, which paves the way for the development of a new class of more predictive microbial ecosystem models.