Bacterial secreted products selectively inhibit non-symbiotic fungi in bees
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Microbial interactions play an important role in shaping microbiome assembly, such as by limiting invasion by harmful organisms that can directly affect the host or disrupt microbiome-associated benefits. Such interactions have been observed across systems, including in the microbiomes of key pollinators such as stingless bees. In Scaptotrigona depilis , bacteria associated with the larval diet inhibit potentially pathogenic filamentous fungi while allowing beneficial yeast symbionts to persist. The mechanisms underlying these effects, however, remain unclear. Here, we combined conditioned media (cell-free supernatant) assays with genomic and metabolomic analyses to investigate whether bacterial secreted products mediate these effects in the bee microbiome. Our results show that bacterial secreted products, particularly from prevalent bacterial taxa such as Apilactobacillus kunkeei , strongly affect fungal growth. Filamentous fungi, including the pathogen Aspergillus , were consistently inhibited, partly through substrate acidification driven by organic acids, but also through additional acidity-independent factors. In contrast, yeast responses were more variable: a non-symbiotic Zygosaccharomyces was inhibited by bacterial metabolites under near-neutral pH, whereas the symbiotic Zygosaccharomyces required for larval development was maintained or promoted under acid-conditioned media. Genomic analyses revealed limited canonical antifungal biosynthetic clusters in the most prevalent bacteria in the larval diet, while metabolomics identified extracellular peptide-like compounds across strains, suggesting a role for non-canonical secreted products. Together, these results show that bacterial secreted products play a key role in selectively shaping fungal communities in the stingless bee larval diet, providing first hints on a mechanistic basis for how microbial interactions structure this ecosystem.
Importance
Microbes associated with hosts or other systems have evolved strategies to persist in their environments, including inhibiting invading microorganisms that could harm their hosts or disrupt the microbial community. In systems where multiple microbial partners coexist, however, these interactions must be selective. The stingless bee Scaptotrigona depilis , for example, hosts bacteria and fungi in its larval diet, where bacteria inhibit fungi outside the core community while allowing required yeast symbionts to persist. Here, we show that this selective fungal inhibition can be mediated by substances released by bacteria, without requiring direct cell-to-cell competition. Bacteria modify the extracellular environment and inhibit potentially harmful fungi, including Aspergillus , through acidification and additional secreted products, while allowing the beneficial yeast to persist. These findings provide a mechanistic basis for selective bacterial-fungal interactions and point to bacterial secreted products as a potential source of yet-uncharacterized molecules with applications in microbial control.
