Can a plant virus make you sick?

29 April 2010

Tabasco virusIt has been estimated that approximately one hundred trillion bacteria colonize the human intestine. That’s about ten times the number of cells that constitute the entire human body. These bacteria are believed to have a mutualistic symbiotic relationship with their hosts. What is known about the viral communities that inhabit our alimentary tract?

The vast majority of DNA viruses in the human gut are bacteriophages, which infect the resident bacteria. The most plentiful RNA viruses in our feces are plant viruses, and the most abundant is pepper mild mottle virus (PMMV). This plant virus is present at high levels, up to  109 virions per gram. The virus has been identified in 12 of 18 fecal specimens taken from healthy humans in the USA and Singapore.

Pepper mild mottle virus is present worldwide in field-grown peppers. It is composed of an RNA genome wrapped with many copies of a viral protein that forms a rod-like particle with helical symmetry (pictured). The origin of PMMV in human feces is the food that we eat. The virus can be readily detected in fresh peppers, and in food products produced from peppers, such as chili powders, sauces, and spices. High levels of PMMV are found in Tabasco sauce, which contains virions that are not only visible in the electron microscope, but which are infectious for plants.

A case-control study was done to test whether presence of PMMV virus in feces is associated with clinical symptoms. Eighteen adults with PPMV positive feces were compared with 31 control, PPMV-negative individuals. Abdominal pain, diverticulosis or diverticulitis, and fever were significantly associated with the presence of PPMV RNA. The authors conclude:  ‘We provide the first evidence that plant viruses may cause disease in humans’. However they admit that ‘clinical symptoms may be imputable to another cofactor, including spicy food’. It’s interesting that 22 of 304 adults, but only 1 of 137 children, were positive for PPMV. The positive child was a 5 year old admitted to hospital because of abdominal pain, fever, asthenia, and hyperventilation. He probably ate too much spicy food, an activity most children don’t engage in.

Could PMMV replicate in human cells? I believe it is highly unlikely. Viruses such as PMMV are transmitted among plants by mechanical means (such as by contaminated farm equipment) and do not enter cells via specific receptors, as do animal viruses. Therefore I see no efficient way for PMMV to enter a human cell. If tomato spotted wilt virus is artificially introduced into HeLa cells, it does not reproduce. However, if the gene encoding the viral RNA polymerase is introduced into HeLa cells along with tomato spotted wilt virus, the viral RNA does undergo replication, although new particles are not produced. These are highly artificial conditions which are unlikely to occur in the human intestine.

The next time you have abdominal cramps after eating spicy food, it’s probably not caused by PMMV, although you will be shedding that virus in your feces. It’s because the chemical constituents of spicy foods affect your digestive tract – in ways that we don’t understand.

Breitbart, M., Hewson, I., Felts, B., Mahaffy, J., Nulton, J., Salamon, P., & Rohwer, F. (2003). Metagenomic Analyses of an Uncultured Viral Community from Human Feces Journal of Bacteriology, 185 (20), 6220-6223 DOI: 10.1128/JB.185.20.6220-6223.2003

Colson P, Richet H, Desnues C, Balique F, Moal V, Grob JJ, Berbis P, Lecoq H, Harlé JR, Berland Y, & Raoult D (2010). Pepper mild mottle virus, a plant virus associated with specific immune responses, Fever, abdominal pains, and pruritus in humans. PloS one, 5 (4) PMID: 20386604

de Medeiros, R. (2005). Expression of a viral polymerase-bound host factor turns human cell lines permissive to a plant- and insect-infecting virus Proceedings of the National Academy of Sciences, 102 (4), 1175-1180 DOI: 10.1073/pnas.0406668102

  • BrianHanley

    About 20 years ago I was at a large party on some property out in the country. I brought my “special brew” with me, a purported “real siberian” recipe for peppar vodka. Unlike what is sold in stores, this vodka was red in color. The recipe was to put 1/4 cup of fresh ground cayenne pepper into a 1 liter bottle and leave it for a year. This is a vodka that one does not every drink until at least 4 shots have gone down. After that, it tastes wonderful, and makes one's heart go thump, which means it is great for dancing all night.

    I doled out shots of this to people, and there was one german man in particular who must have had at least 20 shots. Sometime around 1:00 or 2:00 AM a man I knew came in who hadn't had anything to drink. Drunkenly, I told him no, but he interpreted this as a slight on his manhood, seeing all the other guys crowding around knocking back shots of it. So, I gave him one and he knocked it back like everyone else. Then he screamed, fell on the floor and crawled at a high speed for the food and filled is mouth with sour cream.

    The next morning around 10:00 AM, still drunk, I finally woke up from dreams in which my hand was on fire. I'd wake up and pat it, look and try to go back to sleep. Finally, the pain got so great I sat up and stared at my hand, wondering why this was. Suddenly it hit me, I had been splashing the siberian peppar on my left hand holding people's shot glasses for a couple hours. And then, a terrible thought came over me. I remembered the german man and how he had so many. And I became seriously scared, thinking that if this was what splashing did, maybe I had given him chemical burns in his esophagus.

    Frantically, I called a few physicians I knew, but the had all been at the party too, and weren't answering. Finally, I got hold of a psychiatrist I was friends with, Lee Sanella. He listened calmly, then asked me what kind of pepper it was. I told him it was cayenne from the store. He asked if I was certain, and I went and got a jar like it. He said it would be fine, because it just so happened that when he was a young man doing research at Harvard, prior to becoming a psychiatrist, he had tested cayenne pepper as a potential antibiotic, and worked on isolating compounds in it.

    To do that, he fed chickens 50% of their solid diet by weight as cayenne pepper. Lee said that the chickens were fine, and that it did work as an antibiotic, but only at very high doses. He said that there were other peppers that would cause chemical burns at high concentration, but not cayenne.

    I was very relieved. And I still make that recipe. Some years later, for a while, I decided to habituate myself to it, and at one point I liked eating bananas dipped in a pot of cayenne pepper for breakfast. Wakes you up in the morning better than coffee.

    (Just a story about safety of cayenne pepper in large amounts.)

  • http://www.virology.ws profvrr

    Thanks for that terrific story about cayenne. I'll bet it's full of
    pepper mild mottle virus. I should start now making a batch, since it
    takes a year.

  • BrianHanley

    You're welcome. Will you assay it? :-)
    I suppose one could spin it down at 60K or so for a day, or filter it.

    And I don't do the cayenne bananas anymore. If anyone wants to know if those b pain receptors can grow back, most definitely, they do.

  • gsgs

    how then do plant viruses enter cells ?

  • gsgs

    give humans pepper to eat in different dosages. After some time measure
    the amount of PMMV in the feces. If there is a clear correlation
    between #pepper in and #PMMV out, then it probably doesn't
    replicate in the human. If OTOH few pepper in can give much PMMV
    out then it had replicated.

  • iayork

    To do that, he fed chickens 50% of their solid diet by weight as cayenne pepper.

    Great story, and I assume your German friend survived — but this fact should not have reassured you, because birds don't have the receptors for capsaicin! That means that birds are indifferent to the taste and chemical effects of cayennes, and you can't extrapolate this to humans.

  • BrianHanley

    Yes, the he used birds because rats wouldn't eat it, and it was too much work to force feed them. But the reason it applies to humans is that the stimulation of the b pain receptors is just a stimulation, and not something that causes any actual damage to tissues. So although it hurts and can cause a little irritation in people who aren't acclimated to it, you can safely ignore it. But some other types of peppers have chemistry that can cause some tissue damage. I've never looked into which ones, just taken his word for it.

    The old guy died two weeks ago at 92. I was just told about it yesterday. He had developed cancer when he was 76, it was massively metastasized, so he just decided not to worry about it, went to parties, relaxed lived one day at a time. I visited him about 6 months ago, and we laughed about how odd it was that he had lived so long. He became a headshrinker after getting his MD when he got TB. He could practice with TB as a shrink, but not as an MD then. He was supposed to be roughly a year away from death, and had written himself off when antibiotics came available that cured TB. He went on to do research in psychiatry, wrote what became a seminal little piece titled, “Kundalini, psychosis or transcendence?” and explored the differences and similarities between mysticism and psychosis. Even when he was 90 he would complain about how people had cited him when, “That wasn't what I said at all!” He liked to grouse about “citing me to support things I never dreamed of.” He had a mixed relationship to the psychedelic researchers of his era. He liked a lot of what they did, particularly before Leary came along, and said he saw remarkable, excellent results in ordinary people and seriously ill patients intractable to anything else. He maintained respect for Stan Grof. But he also thought it was blindingly obvious that over-indulgence made some people “flat out bats__t crazy” even if they were still socially healthy, lovable, kind and happy.

    Lee was an unusual combination of very open minded, willing to entertain any possibility, intensely curious, opinionated, perceptive, generous, sometimes to a fault, sometimes irascible and as tough-minded a critic as they come, but able to be kind at the same time. His openness and curiosity got him into hot water and weird situations from time to time. I'll miss the old guy.

    Well, sorry about the impromptu obit, but I really liked him.

  • iayork

    So although it hurts and can cause a little irritation in people who aren't acclimated to it, you can safely ignore it. But some other types of peppers have chemistry that can cause some tissue damage.

    This I didn't know. Thanks.

  • http://agro.biodiver.se/ Jeremy

    Astonishing story. Not going to stop me eating hot peppers though.

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  • wallenmiller

    One little error above: Pepper mild mottle virus (officially abbreviated PMMoV, not PMMV or PPMV) is not structurally similar to TSWV. PMMoV is a tobamovirus which means it has a non-enveloped rod-shaped virion like tobacco mosaic virus (TMV), unlike any human virus. TSWV is in the Bunyaviridae which includes human viruses like Hantavirus and Rift valley fever virus. They all have ambisense RNAs, encapsidated RdRp, and an envelope, unlike PMMoV. Despite this error, I agree w/ all the blogger's conclusions. I suspect it's something other than the plant virus that caused gastric disturbances in some people.

  • http://www.virology.ws profvrr

    I knew that. Corrected, and thank you. And the blogger is me.

  • http://www.virology.ws profvrr

    I knew that. Corrected, and thank you. And the blogger is me.

  • Josh

    As a plant virologist (Ph.D student so I don't get the ologist title yet)…I think there needs to be many more controls done to determine if PMMoV is the culprit….my professional opinion…no way!

  • http://360skeptic.com/ Andrew

    Interesting post. Particularly considering I am at this very moment consuming a lunch smothered in a hot, chipotle pepper sauce.
    Mmmmm. Viruses. Delicious.

  • http://www.phagehunter.org Tim

    I have some doubts about plant viruses actually replicating in our guts. However, it would not surprise me one bit, if we did in fact, have an immune response towards those plant pathogens.

    Other than actual plant virus infection or response to capsacin, the immune response seen to be associated with PMMoV (and perhaps other plant viruses?) could be due entirely to the presence of non-infectious PAMPs that trigger both local and systemic inflammation. Despite not being able to replicate (as far as we know) in human cells, plant viruses still could have plenty of ligands to stimulate various pattern recognition receptors.

  • http://www.virology.ws profvrr

    Good point – there seems to be large amounts of this virus on peppers
    and that could stimulate inflammation. Many of the individuals in the
    Marseilles study also had antibodies against PPMoV, which could occur
    even in the absence of viral replication.

  • Phytodoctor

    how come, if some plant virus can not replicate in human gut, it can infect human???

  • http://www.virology.ws profvrr

    There is no evidence that actual infection has taken place. From the
    intestine, the plant viruses could enter the bloodstream and even
    induce the production of antibodies without replicating.

  • Richnbroke

    If viral affected plant have fruits, would the fruits be virally affected? and if the fruits are affected, would the seeds grow with that particular virus as well?

  • http://www.virology.ws profvrr

    I asked Marily Roosinck (see TWiV #92) and she replied: The answer is,
    if a plant is infected with a virus the fruits can be infected too and
    so can the seeds, but not always. Some viruses get into the seeds and
    others don’t. Viruses that cause symptoms in plants often cause
    symptoms on the fruits too. Some can prevent the seeds from forming
    normally or being viable.

  • http://www.facebook.com/catmarie72 Catherine Marie Conway

    Interesting article and posts. I have three basil plants I was all set to harvest and use towards a big batch of pesto; yum, delicious fresh sumer taste all year long. Sadly I’ve had excessive issues this year with pests, fungi, & disease.  The basil has leaf curl or mosaic virus…transmitted from aphids I believe, amongst other random yet to be identified spots here and there. I love my pesto…but it may be less appealing knowing it carries a plethora of viral or fungal diseases or even worse, can it make me ill? This is what I am trying to discover and what brought me to this article. Most of my findings report transmission between plant and human virus to be unlikely. I guess I will sort through the undesirables and give it a go…I’ve likely consumed much worse with out knowing it. If anyone has any insight into pesto, yay or neigh…give me a hollar.

  • http://topologicoceans.wordpress.com/ charlie

    Interesting article! I 

  • Larry

    My tomatoes have spotted wilt virus and i think i have to kill all the plants, How do i no where it came from and do i have to clean and disinfect everything or do i start new plants and hope it doesnt come back.

  • Ellika

    I’m taking my first Virology course, and as the amateur I am I’m wondering why the plant viruses don’t make us sick? Anyone in the mood for jumping down to my level for a minute?

  • Ellika

    Ah, nevermind!