Scientists say that mass bee deaths may be caused by viruses that disrupt gene expression.
The team analysed which genes were turned on and which were turned off in healthy bees and those from hives with colony collapse disorder (CCD).
Since 2006, CCD has caused the catastrophic loss of US bee hives and is implicated in bee deaths elsewhere.
Writing in PNAS journal, the team say they used "whole genome microarrays" to compare cells from bees' guts.
Lead scientist May Berenbaum from the University of Illinois told BBC News that the research was made possible by publication of the bee genome in 2006.
We talk about a smoking gun. We have the bullet hole! Professor May Berenbaum |
"It's an incredibly useful repository of information which allowed the construction of the microarray - a slide which has all 10,000 bee genes on it," she said.
"We used it to compare colony collapse disorder bees with healthy ones and looked at the differences. There are of course 10,000 genes. So there were a whole lot of differences but we could rule out many of them."
Gut feeling
The team concentrated on analysing gene expression from cells in the bees' guts because this is the primary site of pesticide detoxification and immune defence.
Previous theories for CCD have included pesticide poisoning as well as infection and mite infestation.
But the team's genetic analysis of the bees' guts failed to reveal elevated expression of pesticide response genes.
In addition, genes involved in immune response showed no clear expression pattern despite the increased prevalence of viruses and other pathogens in CCD colonies.
What did show up in the guts of the CCD bees was an abundance of fragments from the ribosome, a structure which is the cell's protein making factory.
According to the researchers, this finding suggests that protein production is likely to be compromised in bees from CCD hives.
Previous research shows that the viruses that bees carry all attack the ribosome.
Little problem
The microbes in question are known as "picorna-like" viruses. The word derives from pico, which means little, and RNA (ribonucleic acid).
"These picorna-like viruses all attack at the same spot," said Professor Berenbaum.
"What they do is to work their way into the ribosome and instead of making honey bee protein they make virus proteins.
"So maybe what's happening is basically the ribosome wears out. So we looked to see if the CCD bees have more of these viruses than healthy bees. And they do.
The viruses in question include "deformed wing virus" and "Israeli acute paralysis virus".
The scientists believe that if a number of similar picorna-like viruses attack simultaneously, they may be able to overwhelm the ribosome.
"We talk about a smoking gun. We have the bullet hole!" said May Berenbaum.
"We now need to look for how multiple viruses might interact on the ribosome."
The honey bee is the US's key agricultural pollinator. As such it is worth $14bn to the country's economy.
CCD was first identified in 2006. In the winter of 2007-8 more than a third of US bees were lost.
Similar losses have been reported in Europe, giving rise to fears that CCD is a global problem.
It turns out, the fungus N. ceranae that was thought to be killing off bee colonies had a partner in crime — a DNA-based virus that worked in tandem with N. ceranae to compromise nutrition uptake in bees:
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http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013181