Manipulating Agaricus bisporus developmental patterns by passaging microbial communities in complex substrates

ABSTRACT There is growing interest in microbiome-based management approaches for plant and animal health and sustainable agricultural practices. To our knowledge, there are no descriptions of Agaricus bisporus mushroom developmental patterns using such an approach. Here, we utilized substrate passaging to select for devomes (developmental microbiomes) in either compost or casing material that resulted in earlier developing (best performing experimental units with a higher number of primordia at day 10 of cultivation) mushrooms compared to unpassaged controls. Passaged casing showed earlier pinning (fruiting body formation), while passaged compost delayed fruiting body formation. Despite changes in pin emergence for passaged substrates and higher mushroom yield in the passaged casing’s first harvest, the total mushroom yield in 24 days of crop cycle did not change significantly. The bacterial communities were distinct between compost and casing materials, but in both microenvironments, the alpha diversity tended to increase and stabilize over time in standard and passaged substrates. Community composition within compost and casing microenvironments tended to be more homogenous after colonization of the fungus. Passaging of casing increased the bacterial alpha diversity and shifted community composition. Such changes were not observed in passaged compost. Some bacterial taxa were enriched or depleted by passaging, e.g., Pseudomonas spp. (hypothesized as a stimulus to A. bisporus fructification) were depleted in passaged compost and casing. Overall, this work presents an experimental approach to manipulate compost and casing microbial communities with the potential to be combined with currently employed cultivation strategies toward a more sustainable mushroom cultivation system. IMPORTANCE Agaricus bisporus is an economically important edible mushroom and manipulating its developmental patterns is crucial for maximizing yield and quality. One of the potential strategies for achieving such a goal is passaging microbial communities in compost or casing. The current study demonstrated that passaging substrates develop enriched microbial communities, and after a few passages, certain levels of changes in mushroom developmental patterns (the timing of fruiting bodies formation) were observed as well as shifts in the bacterial communities. Overall, a better understanding of the complex interactions between microorganisms present in the cultivation system may help farmers and researchers to develop more efficient and sustainable cultivation practices that can both benefit the environment and human health. Agaricus bisporus is an economically important edible mushroom and manipulating its developmental patterns is crucial for maximizing yield and quality. One of the potential strategies for achieving such a goal is passaging microbial communities in compost or casing. The current study demonstrated that passaging substrates develop enriched microbial communities, and after a few passages, certain levels of changes in mushroom developmental patterns (the timing of fruiting bodies formation) were observed as well as shifts in the bacterial communities. Overall, a better understanding of the complex interactions between microorganisms present in the cultivation system may help farmers and researchers to develop more efficient and sustainable cultivation practices that can both benefit the environment and human health.