Bacterial Secretion Systems Contribute to Rapid Tissue Decay in Button Mushroom Soft Rot Disease

The soft rot pathogen Janthinobacterium agaricidamnosum causes devastating damage to button mushrooms (Agaricus bisporus), one of the most cultivated and commercially relevant mushrooms. We previously discovered that this pathogen releases the membrane-disrupting lipopeptide jagaricin. This bacterial toxin, however, could not solely explain the rapid decay of mushroom fruiting bodies, indicating that J. agaricidamnosum implements a more sophisticated infection strategy. In this study, we show that secretion systems play a crucial role in soft rot disease. By mining the genome of J. agaricidamnosum, we identified gene clusters encoding a type I (T1SS), a type II (T2SS), a type III (T3SS), and two type VI secretion systems (T6SS). Through a combination of knockout studies and bioassays, we found that the T2SS and T3SS of J. agaricidamnosum are required for soft rot disease. Furthermore, comparative secretome analysis and activity-guided fractionation identified a number of secreted lytic enzymes responsible for mushroom damage. Our findings regarding the contribution of secretion systems to the disease process expand the current knowledge of bacterial soft rot pathogens and represent a significant stride towards identifying targets for their disarmament with secretion system inhibitors.