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Core Concept Human Health Published: October 12, 2023

The “Friends” That Help Dangerous Bacteria Get Into Your Salad

Abstract

Salmonella enterica is a type of bacteria that can cause vomiting and diarrhea in humans. Normally, Salmonella dies when it is on the surface of healthy plant leaves. However, Salmonella has “friends” on plants that can help it survive. Plant-eating insects and phytobacteria that cause plant diseases can help Salmonella reach new places and access new food sources. Plant-eating insects can move Salmonella from one plant to another and provide Salmonella with valuable nutrients through their poop. Phytobacteria can cause sicken leaves, creating an environment that helps Salmonella enter the leaf and access protection. Both plant-eating insects and phytobacteria can cause leaves to release nutrients that can nourish dangerous bacteria like Salmonella. Together, the combination of Salmonella and insects or phytobacteria on crops may create the perfect recipe for contaminated produce that leads to disease in humans when they eat their healthy fruit or veggies.

What Is a Foodborne Pathogen?

Have you ever gotten really, really sick from eating food? If you had vomiting, stomach pain, and diarrhea, it is likely that you have had foodborne illness. Foodborne pathogens, which are microorganisms that contaminate food, cause these illnesses and make us sick after we ingest them. Just to be clear, not all microorganisms are harmful. There are many microorganisms, including some bacteria within our bodies, that do not cause harm and are necessary for our health. However, some bacteria can cause humans to get sick. In this article, we focus on a type of bacteria called Salmonella enterica (Salmonella), which causes an intestinal infection called gastroenteritis. Several foodborne pathogens can cause gastroenteritis; the specific disease caused by Salmonella is called salmonellosis.

So how does Salmonella end up in the foods we eat? Salmonella commonly lives in the guts of animals such as cows, pigs, and chickens. Unlike us, these animals do not get sick from Salmonella. Salmonella can be transferred from the guts of animals to the parts we eat as food, such as hamburger patties, porkchops, and eggs. Most people are familiar with the connection between salmonellosis and animal products. However, it has become a lot more common nowadays for people to get foodborne illness from fresh produce like tomatoes, sprouts, and leafy greens [1]. Produce like tomatoes are grown in large fields, where Salmonella can exist naturally in the environment. All the steps between the farm field and your dinner plate—including growing in the field, crop harvesting, food processing, and meal preparation—can be chances for Salmonella to get into your food. In the worst situations, major outbreaks of foodborne illness can result in many people ill with salmonellosis. But how does Salmonella first arrive in agricultural fields where our fresh produce is grown and harvested?

Salmonella can live in lots of places; it is naturally found in water and soil and can linger in the environment for a long time without eating. Salmonella directly reaches our crop plants by leaving an animal’s gut through poop, and it can then be transported by water. Contaminated irrigation water (the water used to grow crop plants) has been linked to outbreaks of foodborne illness [2]. During irrigation, water can spray or splash onto leaves and/or fruits, leaving Salmonella bacteria stranded on plants. Surviving on plants is hard for Salmonella, but the bacteria has “friends” that help it cope.

Who Are Salmonella’s Friends on Plants?

When Salmonella arrives on plants, life is stressful because there is no food. Imagine a stray cat wandering around. The cat is likely hungry, thirsty, and uncomfortable, and desperately wants food, water, and shade. Believe it or not, Salmonella has similar problems. Food is scarce for bacteria on plants—the environment is dry, and the bacteria are bombarded by dangerous ultraviolet light from the sun [3]. Stray cats get help from human friends that offer food, water, and shelter. What kinds of friends will drop food scraps for Salmonella?

Insects and phytobacteria, which are bacteria that live on plants, are commonly found in fields where our fruits and vegetables are grown (Figure 1). When insects or phytobacteria attack plants, they transform them into Salmonella-friendly environments. These plant attackers help Salmonella reach new locations and access nutrients. Without its “friends,” Salmonella on plants would slowly die. Let us dive a little deeper into how these friends help Salmonella.

Figure 1 - The crops we grow can be affected by insects and phytobacteria in the field.
  • Figure 1 - The crops we grow can be affected by insects and phytobacteria in the field.
  • Insect feeding can result in visible damage to leaves, and honeydew (poop) left behind can make leaves sticky. Phytobacteria can cause brown spots and yellowing on leaves.

Reaching New Places

From those that pollinate to those that sting, insects are ever-present in our food systems. Insects move around easily and are capable of spreading bacteria. An insect that walks across a leaf contaminated with Salmonella can then walk over to new leaves, moving the bacteria from one leaf to another (Figure 2)—just like someone tracking mud all over your home after playing outside [4]! In addition to walking between leaves, insects can fly over wide distances, dispersing bacteria as they go. Imagine a field heavily infested by insects and recently irrigated with Salmonella-contaminated water. After the insects have explored and fed upon these Salmonella-contaminated plants, some may fly to a faraway field and spread Salmonella there, too.

Figure 2 - Insects and phytobacteria help Salmonella move to new locations, and they create conditions on the leaf surface that help Salmonella to multiply.
  • Figure 2 - Insects and phytobacteria help Salmonella move to new locations, and they create conditions on the leaf surface that help Salmonella to multiply.
  • For example, Salmonella can eat nutrients present in honeydew and nutrients within a leaf water-soaked by phytobacterial disease. Image shows the cross-section (or side-view) of a leaf. Note that objects are not drawn to scale.

The other “friends” of Salmonella, phytobacteria, are very common. Although many phytobacteria are not dangerous to plants, every plant has at least one phytobacteria that can sicken it (plants get sick too!). The diseases caused by phytobacteria can result in brown/dark green spots and yellowing on the surface of leaves, which are visible signs that phytobacteria may be causing a plant to be sick. Phytobacteria are very small—about 100 times smaller than the width of a human hair. However, despite their size, phytobacteria can cause big problems to crop plant, and they can help Salmonella move around by dramatically transforming a leaf into a wet environment (Figure 2) [5].

When some phytobacteria infect leaves, they cause water from the inside of the plant’s cells to leak, creating a wet environment within the leaf interior—you can think of this as plant diarrhea! The water soaking caused by phytobacteria allows bacteria on the outside of the leaf to slide inside through natural openings in the leaf surface called stomata. These stomata serve as the entrance to a sort of “waterslide” that leads to an “indoor pool” created by the water soaking produced by phytobacteria. The distance that Salmonella can travel from the outside of a water-soaked leaf to the inside is quite small compared to the large distances that insects can carry bacteria. However, this change in scenery for Salmonella can make a huge difference. When Salmonella boards the waterslide and rides it into the fabulous, indoor pool, they are protected from harmful dryness and UV light and find a buffet of food.

Snacks for Salmonella

How do insects and phytobacteria provide food for Salmonella? For some insects, it begins with feeding on the contents of a plant’s vasculature, which includes the plant stem and veins that carry nutrients throughout a plant. Scientists have identified over a million insect species with all kinds of unique mouthparts. Leafhoppers use piercing-sucking mouthparts to reach into the plant’s vasculature—think of pushing a straw through a juice box. Thrips, on the other hand, use their ripping-sucking mouthparts to destroy the surface of leaves and then feed on plant cell contents. With the inside of the leaf exposed, food is now available to bacteria that could not access it on their own (Figure 2). This opening in the leaf and cornucopia of available food gives Salmonella protection and a chance to grow, which increases the likelihood of outbreaks of foodborne illness [6].

With eating comes pooping, and insects are no exception. Honeydew (not to be confused with the delicious melon) describes the watery poop produced by insects such as aphids and leafhoppers which only feed on the vasculature of plants. While feeding on the vasculature, insects filter out most of the sugars but some passes through them [7], making their poop as sweet as honey. It even looks like a morning dew drop. Unlike our own poop, insect honeydew does not go to waste. As it is high in sugars, insects (such as ants and bees) and bacteria like Salmonella consume it for food, which helps them to survive on leaves (Figure 2).

Phytobacteria do not leave sugary poop behind like insects do. Instead, they create a nutrient-rich environment. As phytobacteria make plants sick, along with creating a wet environment, they cause plant cells to leak nutrients everywhere! The phytobacteria lounging inside a leaf feast on the sugars and nutrients they caused to leak into the “indoor pool” they created for themselves. Salmonella does not cause plants to get sick, and it cannot construct a sugary, watery pool within leaves by itself. But if phytobacteria have already done that hard work and they are holding open the VIP door (stomata), Salmonella can enjoy all the benefits. When Salmonella reach the sugary insides of phytobacteria-infected leaves, they use the food to multiply, making more and more bacteria (Figure 2) [5]. More Salmonella can mean big problems…

How Might These Friends of Salmonella Affect Us?

Leaves infested with insects or infected by phytobacteria can support higher Salmonella populations compared to healthy plants (Figure 3). Higher Salmonella populations on produce increase the likelihood of foodborne illnesses. Salmonella’s friends on plants—insects and phytobacteria—directly harm food production by reducing a farmer’s harvest, and indirectly harm consumers by increasing the risk of salmonellosis.

Figure 3 - Higher Salmonella populations increase the risk of salmonellosis outbreaks.
  • Figure 3 - Higher Salmonella populations increase the risk of salmonellosis outbreaks.
  • Insect behaviors (such as feeding and pooping) and phytobacteria disease allow Salmonella populations to increase on plant leaves.

There is more than meets the eye when it comes to agricultural fields. Depending on where an insect lands or where a water droplet containing bacteria splashes, the perfect storm for outbreaks of foodborne illnesses can brew. Remember that outbreaks are rare compared to the tons of veggies that are harvested and show up on your plate, so we hope you continue to enjoy your favorite fresh fruits and veggies!

Glossary

Foodborne Illness: Sickness caused by eating food that has been contaminated by a harmful pathogen.

Pathogen: Microorganism that sickens its host; different types can cause harm to humans, animals, and plants.

Microorganism: Tiny organism such as bacteria, fungi, archaea, and viruses that can often be seen only with a powerful microscope.

Gastroenteritis: Illness of the stomach and intestines characterized by vomiting and diarrhea; can be caused by foodborne bacteria and viruses.

Phytobacteria: Microorganisms that live on plants; some types can be pathogenic to plants, causing disease.

Stomata: Microscopic openings in the surface of leaves that are necessary for water vapor, carbon dioxide, and other gasses to enter and exit leaves; can utilized by bacteria to enter leaves.

Vasculature: Network of tubes that carries water, minerals, and food through a plant’s stems, roots, and leaves so it can grow.

Honeydew: Poop produced by insects that feed on the vasculature of plants; contains high amounts of sugar and looks like a clear droplet.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under grant no. DGE-1747503 to MHD and by USDA-HATCH grant no. WIS0322 to JDB and USDA-NIFA grant no. 2016-67017-24422 to JDB and RLG and the Food Research Institute at the University of Wisconsin-Madison to JDB.


References

[1] Dyda, A., Nguyen, P., Chughtai, A. A., and Macintyre, C. R. 2020. Changing epidemiology of Salmonella outbreaks associated with cucumbers and other fruits and vegetables. Glob Biosecur. 1:1–13. doi: 10.31646/gbio.49

[2] Alegbeleye, O. O., Singleton, I., and Sant'ana, A. S. 2018. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review. Food Microbiol. 73:177–208. doi: 10.1016/j.fm.2018.01.003

[3] Teplitski, M., Barak, J. D., and Schneider, K. R. 2009. Human enteric pathogens in produce?: un-answered ecological questions with direct implications for food safety. Curr Opin Biotechnol. 20:166–171. doi: 10.1016/j.copbio.2009.03.002

[4] Soto-Arias, J. P., Groves, R. L., and Barak, J. D. 2014. Transmission and retention of Salmonella enterica by phytophagous hemipteran insects. Appl Environ Microbiol. 80:5447–5456. doi: 10.1128/AEM.01444-14

[5] Dixon, M. H., Cowles, K. N., Zaacks, S. C., Marciniak, I. N., and Barak, J. D. 2022. Xanthomonas infection transforms the apoplast into an accessible and habitable niche for Salmonella enterica. Appl Environ Microbiol. 88:e0133022. doi: 10.1128/aem.01330-22

[6] Harrod, V. L., Groves, R. L., Guillemette, E. G., and Barak, J. D. 2022. Salmonella enterica changes Macrosteles quadrilineatus feeding behaviors resulting in altered S. enterica distribution on leaves and increased populations. Sci Rep. 12:1–13. doi: 10.1038/s41598-022-11750-3

[7] Shaaban, B., Seeburger, V., Schroeder, A., and Lohaus, G. 2020. Sugar, amino acid and inorganic ion profiling of the honeydew from different hemipteran species feeding on Abies alba and Picea abies. PLoS ONE. 15:1–17. doi: 10.1371/journal.pone.0228171