The viruses in your food

cole slawAt the recent Brazilian Virology Society meeting George Rohrmann gave me a copy of his book, Baculovirus Molecular Biology. Baculoviruses are double-stranded DNA containing viruses that infect insects and other arthropods. Early in the first chapter of George’s book I learned that baculoviruses may be present on uncooked cabbage leaves:

…in one study it was found that cabbage purchased from 5 different supermarkets in the Washington D.C. area were all contaminated with baculoviruses to such an extent that each serving (about 100 cm2 of leaf material) would contain up to 108 polyhedra of an NPV pathogenic for the cabbage looper, Trichoplusia ni!

We ingest many other non-animal viruses regularly with foods. In TWiV #79, Red hot chili viruses, we discussed the finding of pepper mild mottle virus, one of the major pathogens of chili peppers, in human feces as well as in pepper or spice-containing food products. Metagenomic analysis of the RNA viruses present in human feces revealed that most viral sequences are similar to plant viruses.  Of 36,769 sequences obtained, 25,040 (91%) resembled plant viruses. In this study, the most abundant human fecal virus was pepper mild mottle virus, present in concentrations of up to 109 virions per gram of dry fecal matter.

The plant (and perhaps insect) viruses that we ingest on a regular basis do not appear to replicate or cause disease in humans. Might they play important roles in development of the immune system, as do the commensal bacteria in our gut?

Zhang, T., Breitbart, M., Lee, W., Run, J., Wei, C., Soh, S., Hibberd, M., Liu, E., Rohwer, F., & Ruan, Y. (2006). RNA Viral Community in Human Feces: Prevalence of Plant Pathogenic Viruses PLoS Biology, 4 (1) DOI: 10.1371/journal.pbio.0040003

Can a plant virus make you sick?

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

TWiV #79: Red hot chili viruses

Hosts: Vincent Racaniello and Alan Dove.

On episode #79 of the podcast “This Week in Virology”, Vincent and Alan converse about making published science accessible to everyone, global eradication of poliomyelitis, and whether a plant virus can cause disease in humans.

This episode is sponsored by Data Robotics Inc. Use the promotion code TWIVPOD to receive $75-$500 off a Drobo.

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Click the arrow above to play, or right-click to download TWiV #79 (51 MB .mp3, 71 minutes)

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