Clay rocks are being considered for radioactive waste disposal but relatively little is known about the impact of microbes on the long-term safety of geological repositories. Thus, a more complete understanding of the microbial community structure and function in these environments would provide further detail for evaluation of the safety of the concept of geological disposal of radioactive waste in clay rocks. It would also provide a unique glimpse into a poorly studied deep subsurface microbial ecosystem. Previous studies concluded that, in pristine Opalinus Clay, microorganisms were present but inactive. In this work, we describe the microbial community and assess the metabolic activities taking place within borehole water. Metagenomic sequencing and genome-binning of a porewater sample containing suspended clay particles revealed a remarkably simple heterotrophic microbial community, fueled by sedimentary organic carbon, mainly composed of two organisms: a Pseudomonas sp. fermenting bacterium growing on organic macromolecules and releasing organic acids and H2, and a sulfate-reducing Peptococcaceae able to oxidize organic molecules to CO2. In Opalinus Clay, this microbial system likely thrives where pore space allows for it. In a repository, this may occur where the clay rock has been locally damaged by excavation or in engineered backfills.