Bee Genome Study Reveals Cause of Colony Collapse Disorder

CHAMPAIGN, Illinois, August 25, 2009 (ENS) - Researchers have found a reliable marker of colony collapse disorder, a mysterious malady that in 2007-2008 killed off more than a third of commercial honey bees in the United States.

University of Illinois entomology professor and department head May Berenbaum and entomology and neuroscience professor Gene Robinson and their colleagues identified a mechanism that could explain the variety of ill effects seen in colony collapse disorder.

Bees in hives affected by colony collapse disorder were found to have unusually high levels of "ribosomal fragments," a symptom of infection with multiple picorna-like viruses.

The study is the first to identify a single molecular marker of the disorder, and to propose a data-driven hypothesis to explain the disappearance of American honey bees.

The research team also included scientists from the U.S. Department of Agriculture, which funded the genome study, published in the current issue of "Proceedings of the National Academy of Sciences."

Colony collapse disorder is characterized by complete absence of adult bees in colonies, with few dead bees in or around the colonies. Bees abandon the colonies, leaving the queen, brood bees that have yet to hatch and food stores of both honey and bee pollen.

Beekeepers have lost hives to the disorder in 24 states, parts of Canada and across Western Europe. Cases have been reported in India, Brazil and Taiwan.

Numerous suspects have been identified in the hunt for a cause of colony collapse disorder, from nutritional deficiencies to exposure to genetically modified plants or pesticides. Researchers in Spain recently pointed to a parasitic fungus, Nosema ceranae, which afflicts many CCD bees in Spain.

The new study made use of the genome and a genome-based tool, the microarray, to look for differences in gene expression in the guts of healthy honey bees and in those from hives afflicted by colony collapse disorder.

University of Illinois scientists May Birnbaum and Gene Robinson with their bees. (Photo courtesy UI)

Such microarray analyses normally identify only active genes – those that have been transcribed into messenger RNA in the first stage of building proteins.

But Reed Johnson, a University of Illinois doctoral student in entomology and first author on the study, noticed that the microarrays were turning up large quantities of fragmented ribosomal RNA (rRNA) in the bees affected by colony collapse disorder.

Ribosomes are the factories in which proteins are made, but Johnson observed that this fragmented rRNA contained adenosine-rich sequences not seen in normal ribosomes - a sign of ribosome degradation.

"Microarrays for other organisms also contain these mysterious pieces of ribosomal RNA, for reasons that are not yet altogether clear," said entomology and neuroscience professor Gene Robinson, a co-principal investigator on the study with entomology professor and department head May Berenbaum.

But comparisons of healthy bees and bees from hives afflicted with colony collapse disorder showed that the fragments were present at a much higher frequency in the CCD bees, he said.

"They are overrepresented in the CCD bees, significantly overrepresented," Berenbaum said. "The one consistent indicator of CCD across samples collected at multiple times and in multiple places was the overabundance of ribosomal fragments."

When the team looked at the pathogens of healthy bees and bees from hives affected by colony collapse disorder, they saw that the CCD bees suffered "more than their share" of infections with viruses that attack the ribosome, Berenbaum said.

These so-called picorna-like viruses "hijack the ribosome," she said, taking over the cellular machinery to manufacture only viral proteins.

The list of picorna-like viruses that afflict honey bees is long and includes Israeli acute paralysis virus, which was once suspected of being the primary cause of colony collapse disorder.

The loss of ribosomal function would explain many of the phenomena associated with colony collapse disorder, Berenbaum said.

"If your ribosome is compromised, then you can’t respond to pesticides, you can’t respond to fungal infections or bacteria or inadequate nutrition because the ribosome is central to the survival of any organism. You need proteins to survive," she said.

The varroa mite, which killed honey bees after it was accidentally introduced to the United States in 1986, is a carrier of picorna-like viruses, and is likely a contributor to the high viral pathogen load that afflicts U.S. bees. The mite may act as a tipping factor leading to ribosome breakdown, the researchers said.

All of these influences, along with the practice of carting bees around the country for pollination services, are significant stressors on the bees, a heavy burden that would be amplified by a loss of ribosomal function, Robinson said.

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