Abundance-activity decoupling in sulfur-cycling bacteria reflects viral infection types in meromictic lakes

Meromictic lakes serve as analogs of redox-stratified ancient oceans with well-mixed surface waters and anoxic bottoms. In sulfide-rich lakes, purple and green sulfur bacteria (PSB, GSB) dominate the anoxic zones where light penetrates, and their biosignatures can guide interpretations of geologic records. Although PSB and GSB biosignatures indicate presence, they do not directly reflect the community composition of modern analog lakes, posing a challenge for interpretation. Here, we investigate this decoupling by integrating metagenomics, metatranscriptomics, and metaHi-C virus-host linkages with the geochemical profiles of three meromictic lakes. In the phototrophic microbial plates, PSB transcriptional activity far exceeded their abundance (73% of total microbial community activity versus 30% of abundance), whereas GSBs displayed the opposite pattern. Concurrently, PSBs were exclusively associated with temperate viruses and GSBs were targeted by lytic infections. Sulfate-reducing bacteria and viruses encoding genes for sulfate reduction were most active where sulfide concentration was lowest. These results reveal that viral replication strategies are associated with the decoupling between abundance and activity in anoxygenic phototrophs and sulfate reducers. These relationships could accelerate sulfur regeneration, contribute to sustaining phototrophy, and ultimately reflect in the lake's bulk biosignatures.