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ARS Home » Pacific West Area » Tucson, Arizona » Carl Hayden Bee Research Center » Research » Publications at this Location » Publication #332048

Title: The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions

item ENGEL, PHILIPP - University Of Lausanne
item KWONG, WALDEN - University Of Texas
item MCFREDERICK, Q. - University Of California
item Anderson, Kirk
item BARRIBEAU, SETH - East Carolina University
item CHANDLER, JAMES - California Academy Of Sciences
item CORNMAN, R. SCOTT - Us Geological Survey (USGS)
item DAINAT, J. - Uppsala University
item DE MIRANDA, J.R. - Swedish University Of Agricultural Sciences
item DOUBLET, J.R. - Martin Luther University
item EMERY, O. - University Of Lausanne
item Evans, Jay
item FARINELLI, L. - Fasteris Sa
item FLENNIKEN, M.L. - Uppsala University
item GRANBERG, M.L. - Uppsala University
item GRASIS, J.A. - San Diego State University
item GAUTHIER, L. - Yale University
item HAYER, J. - Uppsala University
item KOCH, H. - University Of Texas
item KOCHER, S. - Harvard University
item MARTINSON, V.G. - University Of Rochester
item MORAN, N. - University Of Texas
item MUNOZ-TORRES, M. - Lawrence Berkeley National Laboratory
item NEWTON, I. - Indiana University
item PAXTON, R.J. - Martin Luther University
item POWELL, E. - University Of Texas
item SADD, B.M. - Illinois State University
item SCHMID-HEMPEL, P. - Eth Zurich
item SCHMID-HEMPEL, R. - Eth Zurich
item SONG, S.J. - University Of Colorado
item Schwarz, Ryan
item VANENGELSDORP, D. - University Of Maryland
item DAINAT, B. - Agroscope

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/22/2016
Publication Date: 4/26/2016
Citation: Engel, P., Kwong, W.K., Mcfrederick, Q., Anderson, K.E., Barribeau, S.M., Chandler, J.A., Cornman, R., Dainat, J., De Miranda, J., Doublet, J., Emery, O., Evans, J.D., Farinelli, L., Flenbniken, M., Granberg, M., Grasis, J., Gauthier, L., Hayer, J., Koch, H., Kocher, S., Martinson, V., Moran, N., Munoz-Torres, M., Newton, I., Pazton, R., Powell, E., Sadd, B., Schmid-Hempelp., P., Schmid-Hempel, R., Song, S., Schwarz, R.S., Vanengelsdorp, D., Dainat, B. 2016. The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. mBio 7(2):e02164-15. doi: 10.1128/mBio.02164-15.

Interpretive Summary: As pollinators, bees are cornerstones for terrestrial ecosystem stability and key components in agricultural productivity. All animals, including bees, are associated with a diverse community of microbes, commonly referred to as the microbiome. The bee microbiome is likely to be a crucial factor affecting host health. However, with the exception of a few pathogens, the impacts of most members of the bee microbiome on host health are poorly understood. Further, the evolutionary and ecological forces that shape and change the microbiome are unclear. Here, we discuss recent progress in our understanding of the bee microbiome, and we present challenges associated with its investigation. We conclude that global coordination of research efforts is needed to fully understand the complex and highly dynamic nature of the interplay between the microbiome, the host, and the environment. High-throughput sequencing technologies are ideal for exploring complex biological systems, including host-microbe interactions. To maximize their value and to improve assessment of the factors affecting bee health, sequence data should be archived, curated, and analyzed in ways that promote the synthesis of different studies. To this end, the BeeBiome consortium aims to develop an online database which would provide reference sequences, archive metadata, and host analytical resources. The goal would be to support applied and fundamental research on bees and their associated microbes and to provide a collaborative framework for sharing primary data from different research programs, thus furthering our understanding of the bee microbiome and its impact on pollinator health.

Technical Abstract: Fanconi anemia (FA) is a rare genetic disorder caused by defects in DNA damage repair. FA patients often develop squamous cell carcinoma (SCC) at sites where high-risk human papillomaviruses (HPVs) are known to cause cancer, including the cervix. However, SCCs found in human FA patients are often HPV negative, even though the majority of female FA patients with anogenital cancers had preexisting HPV-positive dysplasia. We hypothesize that HPVs contribute to the development of SCCs in FA patients but that the continued expression of HPV oncogenes is not required for the maintenance of the cancer state because FA deficiency leads to an accumulation of mutations in cellular genes that render the cancer no longer dependent upon viral oncogenes. We tested this hypothesis, making use of Bi-L E7 transgenic mice in which we temporally controlled expression of HPV16 E7, the dominant viral oncogene in HPV-associated cancers. As seen before, the persistence of cervical neoplastic disease was highly dependent upon the continued expression of HPV16 E7 in FA-sufficient mice. However, in mice with FA deficiency, cervical cancers persisted in a large fraction of the mice after HPV16 E7 expression was turned off, indicating that these cancers had escaped from their dependency on E7. Furthermore, the severity of precancerous lesions also failed to be reduced significantly in the mice with FA deficiency upon turning off expression of E7. These findings confirm our hypothesis and may explain the fact that, while FA patients have a high frequency of infections by HPVs and HPV-induced precancerous lesions, the cancers are frequently HPV negative.