The Greenhouse Phyllosphere Microbiome and Associations with Introduced Bumblebees and Predatory Mites

Greenhouses are highly productive environments in which conditions are regulated to optimize plant growth. The enclosed character of greenhouses usually results in reduced microbial diversity, while it is known that a diverse microbiome is important for plant health. Therefore, we explored the phyllosphere microbiome of tomatoes and strawberries grown in greenhouses. We observed that the microbiome of both crops was low in diversity and abundance and varied considerably over time and space. Interestingly, the core taxa of tomatoes were Snodgrasella and Gilliamella, genera typically associated with bumblebees. The same amplicon sequence variants (ASVs) were found on reared bumblebees, indicating that the bumblebees, present in the sampled greenhouses to pollinate flowers, had introduced and dispersed these bacteria in the greenhouses. Overall, we found that 80% of plants contained bumblebee-associated taxa, and on these plants, bumblebee-associated reads accounted for up to a quarter of the reads on tomatoes and a tenth of the reads on strawberries. Furthermore, predatory mites had been introduced for the control of spider mites. Their microbiome was composed of a diverse set of bacteria, which varied between batches ordered at different times. Still, identical ASVs were found on mites and crops, and these belonged to the genera Sphingomonas, Staphylococcus, Methylobacterium, and Pseudomonas. These new insights should now be further explored and utilized to diversify ecosystems that are characterized by low diversity and abundancy of microbes. IMPORTANCE Greenhouses, though highly effective agricultural environments, are characterized by reduced sources of bacterial diversity and means of dispersal compared to more natural settings. As it is known that plant health and productivity are affected by associated bacteria, improving our knowledge on the bacterial communities on greenhouse crops is key to further innovate in horticulture. Our findings show that tomato and strawberry crops cultivated in greenhouses harbor poor and variable bacterial communities. Furthermore, commonly implemented biological solutions (i.e., those based on living organisms such as bumblebees and predatory mites) are important sources and means of dispersal of bacteria in greenhouses. This study shows that there is great potential in using these biological solutions to enrich the greenhouse microbiome by introducing and dispersing microbes which have beneficial effects on crop production and protection, provided that the dispersed microbes have a beneficial function.