ARS | Publication request: Proteus mirabilis interkingdom swarming signals attract blow flies

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: December 14, 2011
Publication Date: January 12, 2012
Citation: Ma, Q., Fonseca, A., Liu, W., Fields, A.T., Pimsler, M.L., Spindola, A.F., Tarone, A.M., Crippen, T.L., Tomberlin, J.K., Wood, T.K. 2012. Proteus mirabilis interkingdom swarming signals attract blow flies. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 1:1-11.

Interpretive Summary: Flies and their relatives disperse over 100 pathogens, many of which are responsible for the estimated 76 million food-borne illnesses occurring annually in the U.S. We hypothesized that the behavior of blow flies is influenced by the bacterial communities with which they interact. This influence is called interkingdom signaling, or the communication between organisms from different taxonomic ranks, in this case kingdoms animalia and bacteria. We collected Proteus mirabilis from the salivary glands of the blow fly, Lucilia sericata. Proteus mirabilis is a strain of bacteria which produces a strong odor that attracts blow flies and exhibits a swarming motility, e.g. the movement of a bacterial population across surfaces. Through genetic mutation of six newly identified genes (ureR, fis, hybG, zapB, fadE, and PROSTU_03490), we diminished the swarming ability in several bacteria and demonstrated that it could be restored by the addition of known fly attractants, thus confirming our hypothesis and demonstrating the connection between bacterial swarming and chemical attraction of flies. In addition, bacteria with the swarming mutation, rfaL, were tested for blow fly attraction and attracted fewer blow flies and reduced the number of eggs laid by the flies. Therefore, we have identified several interkingdom signals between bacteria and blow flies which could lead to the identification of chemicals for use in fly control devices, thus reducing pathogen dispersal at concentrated animal feeding operations.

Technical Abstract: Flies transport specific bacteria with their larvae which provides a wider range of nutrients for those bacteria. Our hypothesis was that this symbiotic interaction may depend on interkingdom signaling. We obtained Proteus mirabilis from the salivary glands of the blow fly Lucilia sericat. This strain swarmed significantly and produced a strong odor which attracts blow flies. To identify the putative interkingdom signals for the bacterium and flies, we reasoned that since swarming is used by this bacterium to cover the food resource and requires quorum sensing (QS), the same QS signals used for swarming may be used to communicate with blow flies. Using transposon mutagenesis, we identified six novel genes for swarming (ureR, fis, hybG, zapB, fadE, and PROSTU_03490). Then, confirming our hypothesis, we discovered that fly attractants lactic acid, phenol, NaOH, KOH, and ammonia restore swarming for cells with the swarming mutations. Hence, compounds produced by the bacterium that attract flies also are utilized for swarming. In addition, bacteria with the swarming mutation rfaL attracted fewer blow flies and reduced the number of eggs laid by the flies. Therefore, we have identified several interkingdom signals between P. mirabilis and blow flies.