An illness that has been decimating US honeybees for more than three years probably isn't caused by a single virus, but by multiple viruses that wear down the bees' ability to produce proteins that can guard them against infection, according to a new study.

Image: courtesy of Joseph Spencer

"We may not have the smoking gun," University of Illinois entomologist May Berenbaum, the study's main author, told The Scientist, but "we found the bullet hole."

Cells taken from bees that had succumbed to colony collapse disorder (CCD) were cluttered with ribosomal RNA fragments, suggesting that the bees had trouble translating genetic material into functional proteins, Berenbaum and her colleagues report today (August 24) in the Proceedings of the National Academy of Sciences.

"This is an elegant piece of work that weaves together data on host gene expression, microflora and observations of others into a coherent and compelling story," W. Ian Lipkin, a Columbia University researcher who was not involved with the study, wrote in an email to The Scientist.

Berenbaum and colleagues at the US Department of Agriculture screened thousands of transcripts in the guts of bees from both healthy and CCD-stricken colonies from the east and west coasts of the US.

CCD bees had several unusual RNA fragments resulting from broken, malfunctioning ribosomes. Multiple infections with a family of viruses called the picorna-like viruses, which seem to especially afflict CCD bees, could cause the appearance of such RNA fragments as they overwhelmed ribosomes and limited the cells' ability to manufacture functioning proteins. Bees that are not able to make proteins cannot mount effective responses to viral or bacterial infection or respond to dietary shortages, Berenbaum said.

Although the study didn't uncover a single cause for CCD, said Dan Weaver, a Texas-based apiculturist who was not involved with the research, it "provides some hints and suggestive evidence that maybe there's a general impairment of bees' ability to cope with pathogens at a basic regulatory step."

Berenbaum said that CCD may not be the result of one particular pathogen or environmental factor, but rather may occur when multiple viral infections overwhelm the bees' translational machinery. Bees may be able to handle one or two viral infections simultaneously, but not three or four. "You can recover from a gunshot wound," Berenbaum said, "unless someone is kicking you in the head at the same time."

While apiculturists like Weaver would rather have a single pathogenic cause of CCD in hand, the disorder, which has caused widespread bee mortalities in the US since 2006, appears to be more complex than that. "It would be better if we had more definitive evidence of what exactly is going on," Weaver said. "I think that would be everyone's fervent hope. But so far that hasn't materialized."

Berenbaum's study does, however, rule out some of the previously suggested theories for the cause of CCD. For example, the screen failed to turn up elevated expression of pesticide response genes in CCD bees. "The pattern we saw was inconsistent with pesticides as a cause," said Berenbaum, adding that this will probably not stop some in the honeybee business from blaming pesticide manufacturers for the disorder. Interestingly, the screen also failed to find increased expression of immune response genes, suggesting that the bees were not able to mount effective responses to the pathogens attacking their colonies.

In addition to the ribosomal RNA fragments, Berenbaum's screen revealed a suite of other transcripts, at least one of which resulted from viral infection, which corresponded to CCD. Berenbaum said that she hopes researchers can use these characteristic transcripts and ribosomal RNA fragments to develop a way to rapidly identify bees struck with CCD. "At the very least we have markers that we think is a reliable and objective indicator of CCD," she said. "Ultimately we can have a quick assay that would allow a more objective analysis of CCD."

Weaver welcomed the idea, but lamented the pace at which scientists are able to fully understand CCD. "I'm happy that we're making progress," he said. "It's just painfully slow."


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