Detection, Detrimental Effects, and Transmission Pathways of the Pathogenic Bacterium Acaricomes phytoseiuli in Commercial Predatory Mites

Arthropod pathogens and other microorganisms have been documented from mass production systems aimed at producing natural enemies for pest control. If losses due to pathogens are encountered in such systems, they could lead to uneconomical production of natural enemies and/or a loss of predator quality for effective field control of target pests. Here, we identify and describe the laboratory transmission of a bacterial pathogen, Acaricomes phytoseiuli, in a Chinese strain of the local predatory mite Neoseiulus californicus following contact with Phytoseiulus persimilis, a predatory mite imported for the control of small sap-sucking pests in greenhouses. Analysis of the 16S rRNA gene and whole-genome sequences of A. phytoseiuli isolated from the Chinese strain of N. californicus showed 99.6 and 99.78% similarity, respectively, to the pathogen isolated from a European population (DSM14247 strain). This is the first report of P. persimilis infected with A. phytoseiuli outside Europe and transmitting to a local predatory mite species. A. phytoseiuli severely damaged local N. californicus, leading to a dorso-ventrally flattened body and reduced prey consumption and reproduction as well as early death. Through fluorescence in situ hybridization, A. phytoseiuli was shown to accumulate in the digestive tract of mites and in the oviductal bulb of adult females. Infected males had no obvious symptoms, but they still were able to pass on the infection to healthy females through contact and mating. The pathogen was transmitted vertically to offspring by either infected parent through adherence to eggshells. A. phytoseiuli could also persist in other herbivorous arthropods from the same habitat, suggesting wider potential risks. Our study highlights pathogen risk to predators in local biocontrol industries through pathogen spread from imported material. IMPORTANCE Predatory mites are important natural enemies for biological control of pests, but mass rearing of the mites can be affected by pathogens. In particular, the mite pathogen Acaricomes phytoseiuli may pose a threat to predatory mite production, and we have now detected this pathogen in China. We explored the pathogen's transmission within species, its ability to transfer to a locally important predatory mite species, and symptoms following transfer. The detection of A. phytoseiuli and its ability to transfer to a local predator where it reduces performance highlight the importance of ongoing monitoring and hygiene in the predatory mite industry.