Proteorhodopsin (PR) is a microbial proton pump that plays a significant role in phototrophy of bacteria in marine environments. Fundamental understanding of the structure-function relationship that drives proton pumping in PR has largely been elusive due to a lack of high-resolution structures of the photointermediates in the PR photocycle. Extending upon previous work, we used long-time scale molecular dynamics (MD) simulations to characterize the M state of the blue variant of PR, which represents the first proton transfer that takes place in the photocycle. Several notable structural changes occur in the M state that are hallmarks of subsequent steps in the PR photocycle, indicating that although this protein is often compared to the canonical microbial rhodopsins, such as bacteriorhodopsin, PR possesses characteristics that make it distinct among the rapidly increasing and widely variable catalog of microbial rhodopsins.