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Suspicious Virus Makes Rare Cross-Kingdom Leap From Plants to Honeybees

The views expressed are those of the author and are not necessarily those of Scientific American.


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Tobacco ringspot virus extracted from honeybees. Adapted from Fig. 2 from Li et al., 2014. Click image for source.

When HIV jumped from chimpanzees to humans sometime in the early 1900s, it crossed a gulf spanning several million years of evolution. But tobacco ringspot virus, scientists announced last week, has made a jump that defies credulity. It has crossed a yawning chasm ~1.6 billion years wide.

And this is likely bad news for its new host, the honeybee, matchmaker of crops and bringer of honey.  These are two services for which humans are both eternally indebted, and, in the case of the former, possibly unable to live without. Bees pollinate the majority of our fruit and nut crops and many vegetables — some 90 all told — without which humanity would be nutritionally impoverished. Yet shortages are a possibility we are confronting, as bee populations in America have declined in recent years for reasons that seem to be both diverse and elusive. Colony collapse disorder, as whatever it is is called, was first reported in 2006 and has spread globally. Many viruses, parasites, and pesticides have been implicated, but no smoking gun has emerged.

As scientists were studying the possible role of pollen in spreading known bee viruses, a team of scientists from the United States and China began screening bees and pollen for viruses of all sorts. To their surprise, as they reported Jan. 21 in the journal mBio, they discovered a common plant virus — tobacco ringspot virus — had seemingly infested honeybees. Was it merely a transient visitor? Or had it made itself at home in a place inconceivably different from its usual digs?

Their first clue was the virus’s genome. Tobacco ringspot virus is an RNA virus. Though DNA acts as a stable repository of instructions for building proteins, RNA is how that information is transmitted to the part of the cell that manufactures them. It is transient by nature, and recycled after a short time. As a result, RNA polymerase, the enzyme that makes RNA by copying DNA, is not as careful as DNA polymerase, the enzyme that replicates it. It lacks a key proofreading mechanism that DNA polymerase has (3′->5′ proofreading), and as a result, is more likely to make mistakes called mutations. In humans, that is not a problem, because the life of an individual strand of RNA is brief and any mistakes end with its destruction.

But for RNA viruses, their hereditary information is RNA, and the extremely high RNA virus mutation rate is a powerful engine of evolution. It generates the diversity on which natural selection can act.  Mistakes can lead quickly to deformed or malfunctioning virions (no big deal for viruses) or to new host conquests (big deal for viruses) alike. RNA viruses have generated many celebrities; HIV is an RNA virus, as are SARS  and influenza. RNA viruses are the most likely source of host-jumping viruses or an infection that suddenly acquires greater virulence, the authors of the study said.

Still, a leap between kingdoms is not an everyday event. Most plant viruses do rely on plant-eating insects to swap hosts. But very few of them actually infect those insects. One exception is the Rhabdoviridae, the family of viruses that includes rabies. Some viruses in that family have long been known to infect both plant and animal hosts.

In spite of its name, tobacco ringspot virus infects many plants besides tobacco from more than 35 families, including tomato, cucumber, beans, and many woody plants. This is a virus that loves plants, although they assuredly don’t love it back. It can stunt or kill the plant, possibly discoloring the leaves in a characteristic ringspot pattern in the process.

Symptoms of tobacco ringspot virus on burley tobacco, Nicotiana tabacum. Tobacco ringspot infects many plants besides tobacco, most seriously soybean. R.J. Reynolds Tobacco Company Slide Set, R.J. Reynolds Tobacco Company, Bugwood.org. CC by 3.0, via IPM Images. Click for source and license.

Tobacco ringspot virus is spread between plants in any number of ways — the virus is not picky. It can be transmitted directly to the next generation by infected seed. Or it can be passed from one plant to another by a dagger nematode, a tiny soil worm with a piercing stylus for sucking plant juices. Any number of other plant-sucking or leaf-eating insects can do the job, too: aphids, thrips, grasshoppers, or tobacco flea beetles, perhaps. Or honeybees. The bees can spread the virus to a new plant via infected pollen.

Which brings us back to the mysterious matter of the plant virus that appeared in a bee, how it might have gotten there, and what it might be doing. Bees handle pollen in some fairly intimate ways. Their bodies are electrically charged so that pollen sticks, but they also carry baskets on their hind legs into which they stuff gobs of the stuff. Then, back at the hive, they mix the pollen into “bee bread”, by combining it with honey and their own glandular secretions, which they may later eat. In short, bees wallow in pollen like hogs in slop, ensuring that any enterprising pollen-borne viruses have both means and motive to make a host leap. Whether the virus had established long-term residency in its new host was unknown, though.

The scientists sampled tissue from throughout the bees’ bodies to see if was concentrated in their gut and salivary glands, where it would be most expected if it was just passing through. They found something very different. The virus did not appear to replicate at all in their guts or salivary glands, and very few virus particles were found there. Instead, the virus had spread throughout bees’ bodies and replicated particularly well in their wings, nerves, antennae, trachea, and blood (technically, hemolymph). Ominously, it seemed to especially favor nervous tissue. Far from being a polite and unintrusive guest, it looked like the virus had picked the front door lock, raided the fridge and keg, and called to start the cable TV.

But the news for bees got worse. When the scientists looked inside the mites Varroa destructor, which have been implicated in colony collapse disorder and make a living as a nasty tick-like parasite of bees (if ticks were the size of dinner plates), their guts were full of tobacco ringspot virus. As with ticks, Varroa mites sap their hosts’ energy and are known to spread disease. But unlike the bees, the mites’ tobacco ringspot infections were limited to their gut, vastly decreasing the possibility of a silver lining in which the virus preyed on bee parasites as well as bees.

To see what the viruses themselves might reveal about what had happened, the scientists compared tobacco ringspot genes from plants, bees, and mites. The viruses in bees and mites were closely related, implying the mites picked up the virus from the bees, and that they both came by their virus via a common ancestor — a single ill-starred encounter between a particular bee and a particular grain of pollen, perhaps. Moreover, bee pollen stashed in the hive — that “bee bread” stuff mentioned earlier — was contaminated with the same strain.

But the presence of virus alone throughout bee bodies doesn’t reveal whether the virus is causing harm. So the scientists sampled six strong and four weak hives of bees over the course of a year in order to see whether tobacco ringspot might be having any deleterious effects on its new mobile home. They looked for that virus and a variety of other viruses implicated in colony collapse disorder — among them, Deformed Wing Bee Virus (DWV), Black Queen Cell Virus (BQCV), and Israel Acute Paralysis Virus (IAPV). Indeed, higher concentrations of tobacco ringspot and these other viruses seemed to presage colony collapse.

Fig. 5 from Li et al., 2014. Click image for source.

Many other unknowns remain. The team doesn’t know if the virus can persist in bees without frequent re-introduction from pollen. They also don’t know if the bees can give the virus back to uninfected plants. And of course, whether these suspicious viruses are jointly the cause of collapse, a symptom of some other underlying malady (weakened bees may be more prone to viral infection), or both, remains difficult to say. The story of colony collapse disorder remains unfinished.

It’s worth reflecting on why this particular viral invasion is so remarkable. A virus wishing to conquer any new host — much less one separated from the established host by more than a billion years of evolution — must overcome several substantial obstacles. It must encounter the new host. Its coat proteins must evolve such that they permit it to gain entry to hosts’ cells, although a change to one or a few protein subunits called amino acids may be enough to get the job done. Then, the virus’s genome must evolve to let it evade its new host’s immune system and hijack its cellular replication machinery. Finally, the virus must find a way to spread from one new host to another. It’s a tall order, and that tobacco ringspot appears to have accomplished it all seems extraordinary.

According to the authors of this study, this is the first evidence that honeybees can be infected by plant-virus contaminated pollen, but it might not have been the first or last. About 5% of plant viruses are pollen-borne. The genetic material of most? RNA.

Reference

Li J.L., Cornman R.S., Evans J.D., Pettis J.S., Zhao Y., Murphy C., Peng W.J., Wu J., Hamilton M. & Boncristiani H.F. & (2013). Systemic Spread and Propagation of a Plant-Pathogenic Virus in European Honeybees, Apis mellifera, mBio, 5 (1) e00898-13-e00898-13. DOI:

Jennifer Frazer About the Author: Jennifer Frazer is a AAAS Science Journalism Award-winning science writer. She has degrees in biology, plant pathology/mycology, and science writing, and has spent many happy hours studying life in situ.
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Follow on Twitter @JenniferFrazer.

The views expressed are those of the author and are not necessarily those of Scientific American.





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  1. 1. Silkysmom 4:56 pm 01/31/2014

    Yet shortages are a possibility we are confronting, as bee populations in America have declined in recent years for reasons that seem to be both diverse and elusive. Colony collapse disorder, as whatever it is is called, was first reported in 2006 and has spread globally. Many viruses, parasites, and pesticides have been implicated, but no smoking gun has emerged.

    Maybe if the beekeepers didn’t feed their bees high fructose corn syrup the bees would be healthy enough to fight off disease. If you took food away from your kids and just fed them garbage, how would they fare?

    Link to this
  2. 2. Cairenn 8:53 pm 01/31/2014

    CCD was NAMED then, it has been reported for many years before. In fact there are reports from the Roman empire around the time of Christ that describes it.

    European honeybees are not native to the Americas, they are an imported species.

    Link to this
  3. 3. Gorden Russell 9:39 pm 01/31/2014

    Could it be that an artificial compound served as a mutagen (as in insecticides or herbicides or other chemicals used on farms) and that mutagen allowed the virus to make this big jump?

    Link to this
  4. 4. natetrask 9:56 pm 01/31/2014

    Time for Nano-tech/drones…

    Link to this
  5. 5. xirrad 2:17 am 02/1/2014

    spelling and grammar: 1900s, not 1900′s

    Link to this
  6. 6. MaxPen 7:03 am 02/1/2014

    This is quite shocking!

    Link to this
  7. 7. Jennifer Frazer in reply to Jennifer Frazer 9:00 am 02/1/2014

    xirrad — thanks for pointing that out. Fixed!
    Gorden — I’m not enough of a colony collapse expert to speculate on that. I’ve heard so many different things!
    Cairenn — scattered incidents resembling the symptoms of colony collapse has long been reported from bees, I think. But they could have had different causes over time. This particular *widespread* manifestation/pattern of collapse was not reported until 2006, according to the mBio article I wrote about.

    Link to this
  8. 8. enyaroedelius 3:38 pm 02/1/2014

    Save the honeybee!

    http://www.youtube.com/watch?v=rI3gsb_d27I

    Link to this
  9. 9. edrybicki 4:48 am 02/3/2014

    I will be blogging in detail on this later – with the assistance of the esteemed Adrian Gibbs – but I think it is necessary to point out a couple of things here.
    First, nice analysis and very informative.
    Second, though…you say
    “A virus wishing to conquer any new host — much less one separated from the established host by more than a billion years of evolution — must overcome several substantial obstacles”
    Ummm….I have pointed out elsewhere that plants and insects are a lot more intimately connected than people realise, evolutionarily, and there are in fact a significant number of cross-kingdom jumps that have occurred.
    Consider, for example, that plant rhabdoviruses and bunyaviruses almost certainly originated in insects, and still infect them – but others also infect mammals, indicating that a subsequent evolutionary divergence of insects and in their feeding targets could satisfactorily account for everything.
    Which means that the evolutionary gulf the article discusses is nothing like a billion years, as it in fact dates back to when insects and plants were the only higher organisms on dry land – to be joined by reptiles later.

    Link to this
  10. 10. edrybicki 5:08 am 02/3/2014

    Further to Big Jump viruses, from my teaching material:
    “A complicating factor in the picture of viruses co-evolving with their hosts over millennia is the fact that viruses apparently can – and obviously do – make big jumps in hosts every now and then. It seems obvious, for example, that arthropods are almost certainly the original source for a number of virus families infecting insects and mammals – such as the Flaviviridae – and probably also of viruses infecting insects and other animals and plants – such as the Rhabdoviridae and Reoviridae – as well (see also here). For example, picornaviruses of mammals are very similar structurally and genetically to a large number of small RNA viruses of insects and to at least two plant viruses, and – as the insect viruses are more diverse than the mammalian viruses – probably had their origin in some insect that adapted to feed on mammals (or plants) at some distant point in evolutionary time.”

    Link to this
  11. 11. Jennifer Frazer in reply to Jennifer Frazer 4:34 pm 02/3/2014

    ed — Thank you for your kind words. The evolutionary gulf I refer to in this article has nothing to do with the virus. It is the amount of evolutionary time separating the two hosts — that is, the amount of time since animals and plants last shared a common ancestor. As discussed here, it’s around 1.6 billion years.

    Link to this
  12. 12. edrybicki 10:19 am 02/4/2014

    Sure! But the viruses have been associating with both the hosts since well after their separation – because insects have been feeding on / associated with plants for only 500 million-odd years, since they met after separately crawling out of the water.
    Whatever, it’s a great area for speculation and yours is a great article.
    More!

    Link to this

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