Are Biocontrols for Plant Diseases Safe to Humans?

I recently received a phone call from a citizen sounding quite frightened about an unusual bacterial infection she was experiencing.  Her physician had diagnosed the infection to be due to the bacterium, Pantoea agglomerans.  I did my best to answer her questions, primarily informing her how widespread and common this bacterium can be on plant surfaces and in soil.

As I thought about this case, the thing that most struck me was that P. agglomerans (which has been known by several scientific names) has been widely studied as a potential biocontrol agent for plant diseases.  As I dug into the scientific literature, I learned about many cases of P. agglomerans causing opportunistic infections in humans, often (though not always) associated with immunosuppression.

“Wait a minute!” I thought.  You mean, this natural biocontrol agent, which we commonly assume is nothing but beneficial, could actually cause harm to humans?  Most field plant pathologists are well-aware of the mistaken—but widely held—assumption that synthetic chemicals are harmful while natural chemicals are safe [1].  This isn’t the first time I have wondered about the safety of microbial biocontrol agents.  However, this was the first time I had ever “drilled down” into the scientific literature on this topic.

There was more there than I expected.  A number of bacterial species that can provide some biological control of plant disease have indeed been shown to be opportunistic human pathogens.  The ones I read about are listed below, with citations to some of the medical literature associating them with human infections:

  • P. agglomerans [2, 3];
  • Stenotrophomonas maltophilia [4];
  • Bacillus cereus [5];
  • Bacillus subtilis [6];
  • Lysobacter enzymogenes [7].

My literature search was not at all exhaustive.  Therefore, there could even be additional examples of biocontrol bacteria with “alter-egos” as opportunistic pathogens in humans.

There is a significant caveat.  Even though a bacterial species may be reported both in human infections and as a plant colonist, the human strains and the plant strains may not necessarily come from the same populations [8].  But I don’t take much comfort in that, for the following reasons:

  1. Relatively recent studies suggest that some of the human-infecting and plant-colonizing strains of P. agglomerans seem worryingly similar [9, 10].
  2. Even if they are from different populations, the classification of the human-infecting and plant-colonizing strains as the same species indicates that they have some phenotypic overlap.

To be honest, my discoveries concern me much more than traces of synthetic pesticides in my food.  And to think that farm workers sometimes apply biocontrol agents with no safety equipment!

So the take-away is, our concern for food safety should be in proportion to scientific risk, and not based on assumptions.  Biocontrol agents for plant disease control, sometimes assumed to be safe because they derive from Nature herself, may not be as safe as we think.  Likewise, pesticides—whether natural or synthetic—should not be assumed to be safe.

We do a good job evaluating pesticide safety in the USA, through intensive and increasingly sophisticated scientific and regulatory procedures.  Our pesticides undergo such extensive safety testing that, while I wash my produce well, I don’t concern myself with parts-per-billion—or parts-per-trillion—of pesticides in my food [11].  But my safety “radar” is up now on biocontrol agents.  Some questions worth asking:

  • What kind of safety testing do biocontrol agents undergo?
  • How good is our knowledge of exposure routes and doses?
  • Are they tested against immunocompromised mammals?
  • Are they tested for chronic effects?
  • What else do we need to know about biocontrol agents in order to assure the safety of our food supply, as we seek to reduce the use of synthetic pesticides by using alternative, “natural” materials?

 

Literature cited

  1. Ames, B. N., Profet, M. and Gold, L. S., Dietary pesticides (99% all natural). PNAS, 1990, Vol. 87, p. 7777-7781. Available from: http://www.pnas.org/content/87/19/7777.full.pdf
  2. Dutkiewicz, J., Mackiewicz, B., Lemieszek, M. K., Golec, M. and Milanowski, J., Pantoea agglomerans: a marvelous bacterium of evil and good .Part I. Deleterious effects: Dust-borne endotoxins and allergens – focus on cotton dust. Ann Agric Environ Med, 2015, Vol. 22, p. 576-88, DOI: 10.5604/12321966.1185757. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26706959
  3. Cruz, A. T., Cazacu, A. C. and Allen, C. H., Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol, 2007, Vol. 45, p. 1989-92, DOI: 10.1128/JCM.00632-07. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17442803
  4. Brooke, J. S., Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev, 2012, Vol. 25, p. 2-41, DOI: 10.1128/CMR.00019-11. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22232370
  5. Bottone, E. J., Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev, 2010, Vol. 23, p. 382-98, DOI: 10.1128/CMR.00073-09. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20375358
  6. Oggioni, M. R., Pozzi, G., Valensin, P. E., Galieni, P. and Bigazzi, C., Recurrent septicemia in an immunocompromised patient due to probiotic strains of Bacillus subtilis. Journal of Clinical Microbiology, 1998, Vol. 36, p. 325–326. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC124869/
  7. Dempsey, K. E., Riggio, M. P., Lennon, A., Hannah, V. E., Ramage, G., Allan, D. and Bagg, J., Identification of bacteria on the surface of clinically infected and non-infected prosthetic hip joints removed during revision arthroplasties by 16S rRNA gene sequencing and by microbiological culture. Arthritis Res Ther, 2007, Vol. 9, p. R46, DOI: 10.1186/ar2201. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17501992
  8. Bonaterra, A., Badosa, E., Rezzonico, F., Duffy, B. and Montesinos, E., Phenotypic comparison of clinical and plant-beneficial strains of Pantoea agglomerans. 2014, Vol. 17, p. 81-90, DOI: 10.2436/20.1501.01.210. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26418852
  9. Volksch, B., Thon, S., Jacobsen, I. D. and Gube, M., Polyphasic study of plant- and clinic-associated Pantoea agglomerans strains reveals indistinguishable virulence potential. Infect Genet Evol, 2009, Vol. 9, p. 1381-91, DOI: 10.1016/j.meegid.2009.09.016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19800991
  10. Rezzonico, F., Smits, T. H., Montesinos, E., Frey, J. E. and Duffy, B., Genotypic comparison of Pantoea agglomerans plant and clinical strains. BMC Microbiol, 2009, Vol. 9, p. 204, DOI: 10.1186/1471-2180-9-204. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19772624
  11. Winter, C. K. and Katz, J. M., Dietary exposure to pesticide residues from commodities alleged to contain the highest contamination levels. J Toxicol, 2011, Vol. 2011, DOI: 10.1155/2011/589674. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21776262

 

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6 thoughts on “Are Biocontrols for Plant Diseases Safe to Humans?

  1. Thank you for sharing this! From my own side project, some endophytic bacterial isolates from the Bacillus cereus clade express enterotoxin genes when grown in pure culture. I think that a portion of the community have fallen into the “its natural, so safe” mentality. Radon is natural, but we know of all the issues it causes. In my job as an editor, I occasionally see manuscripts screening known human pathogens for immunocompromised individuals or even species that might be mycotoxin producers screen as biological control agents! I think the first screening should be to determine species and then tossing anything known to be a potential problem for human health.

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    1. Thanks for your comment. I honestly don’t know how to design a screening program for potential biocontrol agents, but you approach seems reasonable: screen first for potential pathogens, and discard those candidates.

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    2. I am still puzzling over this topic. Figure 1 in the following paper shows that Bacillus strains may possess both desirable genetics (cry protein conferring biopesticidal properties) and one or two virulence plasmids (Genomic insights into the taxonomic status of the Bacillus cereus group, http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4571650/). This seems consistent with our shared concern over potential virulence of biocontrol strains.

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