BLOOMINGTON, Ind. -- An Indiana University researcher and collaborators have published the first comprehensive analysis of the gut bacteria found in queen bees.

Despite the important role of gut microbial communities -- also known the "microbiome" -- in protecting against disease, as well as the central role of the queen bees in the proper function and health of the hive, similar analyses of honey bees have previously only been performed on worker bees.

Apis mellifera -- or the western honey bee -- contributes significantly to agriculture, including pollinating one out of every three mouthfuls of food globally. Understanding the role of microbes in the productivity of queen bees and health of bee colonies may provide critical insights into the decline of bees in recent years, with colony losses as high as 40 percent over winter.

The research, "Characterization of the honey bee microbiome throughout the queen-rearing process," appears online and will appear in print in the journal Applied and Environmental Microbiology. Also contributing to the study were researchers at Wellesley College and North Carolina State University.

"This might be a case in which 'mother does not know best,'" said Irene L.G. Newton, assistant professor of biology in the College of Arts and Sciences' Department of Biology at IU Bloomington, who is corresponding author on the study. "In many animals, transmission of the microbiome is maternal. In the case of the honey bee, we found that the microbiome in queen bees did not reflect those of worker bees -- not even the progeny of the queen or her attendants. In fact, queen bees lack many of the bacterial groups that are considered to be core to worker microbiomes."

The study's results are the opposite of microbiome development in many mammals, including humans, in which infants' microbiomes are influenced by their mothers. Babies delivered through natural birth possess microbiomes similar to those found in their mother's birth canal, for example, while babies born through cesarean section harbor gut bacteria that resemble bacteria found on the skin.

Honey bees, in contrast, acquire their gut bacteria from both the surrounding environment and the social context -- a phenomenon known as horizontal transmission.

In a healthy colony, worker bees typically acquire their gut bacteria through interaction with microbes inside the hive, including fecal matter from adult bees. But the most likely route of microbiome transmission in queen bees is the "royal jelly," protein-rich food source produced by worker bees and responsible for the development of queen bees during the larval stage. Unlike other bees, queens continue to feast on royal jelly through maturity, eschewing the honey and "bee bread" consumed by workers.

The queen's royal isolation from the dirt and grime of everyday life in the colony may account for the difference in her microbiome.

"In some ways, the development of the queen microbiome mirrors that of workers, with larval queens' associated bacteria resembling those found in worker larvae," Newton said. "But, by the time they mature, queens have developed a microbial signature distinct from the rest of the colony."

Newton's study tracked the development of the queen microbiome at every point in the commercial rearing process -- from the larval stage to their emergence as adults capable of reproduction. The scientists also tracked worker populations interacting with the queens at each point in their development, including the queens' introduction to new colonies, a common practice in commercial beekeeping. At the end of the process, DNA collected from the honey bees' guts were sequenced and analyzed.

Sequencing was performed at the Indiana Center for Genomics and Bioinformatics in Bloomington, Ind., as well as in Massachusetts. The field research, including honey bee collection, was conducted at the North Carolina State University Lake Wheeler Honey Bee Research Facility in Raleigh, N.C.

The study's discovery that queen bees' microbiome remains unaffected by workers' interaction with the queen, and by the movement of queens to different colonies, suggests that modern beekeeping practices -- in which queen bees are regularly removed from their home colonies and introduced into new hives -- may not detrimentally affect the health of the colony.

"Because the queen microbiome does not reflect the workers within a specific colony, the physical movement of queens from one colony environment to another does not seem to have any major effects on either the queen gut or worker gut communities," she said. "The research provides no evidence that beekeepers who regularly replace their queens from outside genetic sources harm their colonies by disrupting the gut microfauna of a particular colony. In many ways, these conclusions are very reassuring for the commercial-production apiculture industry."

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In addition to Newton, authors on the study are David R. Tarpy of the W.M. Keck Center for Behavioral Biology at North Carolina State University and Heather R. Mattila of the Department of Biological Sciences at Wellesley College.

This work was supported by a grant from the National Honey Board, as well as support from the Knafel Endowed Chair in the Natural Sciences at Wellesley College.