The permanently anoxic waters in meromictic lakes create suitable niches for the growth of bacteria using sulphur metabolisms like sulphur oxidation. In Lake Pavin, the anoxic water mass hosts an active cryptic sulphur cycle that interacts narrowly with iron cycling, however the metabolisms of the microorganisms involved are poorly known. Here we combined metagenomics, single‐cell genomics, and pan‐genomics to further expand our understanding of the bacteria and the corresponding metabolisms involved in sulphur oxidation in this ferruginous sulphide‐ and sulphate‐poor meromictic lake. We highlighted two new species within the genus Sulfurimonas that belong to a novel clade of chemotrophic sulphur oxidisers exclusive to freshwaters. We moreover conclude that this genus holds a key‐role not only in limiting sulphide accumulation in the upper part of the anoxic layer but also constraining carbon, phosphate and iron cycling.