Sniff Test: Bacteria May Have a Primordial Sense of Smell

A study suggests that bacterial colonies can detect and respond to airborne ammonia

Reindert Nijland and J. Grant Burgess, Newcastle University

Bacteria can really stink. It is a truth acknowledged by anyone whose nostrils have confronted a carton of curdling milk or a pair of socks still saturated with memories of a marathon. But a new paper suggests that bacteria do not just reek odor—they also can smell it. Bacterial colonies detect pungent ammonia molecules released by neighboring colonies and respond by coating themselves in protective slime, according to a study published August 11 in Biotechnology Journal (BTJ). Not only is this the first evidence for a sense of smell in bacteria, the results also might represent one of the earliest forms of olfaction in evolutionary history.

"It's an interesting paper," says Vanessa Sperandio, a microbiologist at the University of Texas Southwestern Medical Center at Dallas who was not involved in the study. "Bacteria don't smell like multicellular organisms that have noses, but it could be a primitive form of what developed later. I think it's the first time someone has shown that bacterial cells can actually sense odorous gases like ammonia. But it's not the first time that we've shown bacteria can sense gases. Bacteria can detect oxygen, for example."

Bacteria also release, detect and respond to organic signaling molecules in a process known as quorum sensing. The authors of the new paper distinguish between olfaction—or smelling—and quorum sensing in that the latter usually involves molecules exchanged between bacteria within a shared liquid medium, whereas the former involves volatile (airborne) molecules, subsequently detected by different colonies separated by a physical barrier.

The BTJ study arose as something of an accident. The researchers were not specifically invested in studying how bacteria respond to airborne molecules—at first. Rather, they were trying to learn how bacteria produce biofilm—a kind of structured slime that enables microorganisms to adhere to surfaces, band together and block out competitors in their immediate environment.

"Biofilm is like a city for bacteria to live in," Sperandio says. "The bacteria secrete a slimy matrix and organize themselves into a multicellular structure with channels for water and nutrients to flow in and out."

To save space in the laboratory, the researchers decided to create two kinds of growing conditions for the common soil bacterium Bacillus licheniformis using a single microtiter plate—a plastic tray with 96 little wells. In all the wells on the left side of the plate the researchers grew bacteria in a complex nutrient-rich medium; in the right half they used a medium that contained fewer nutrients, but was specifically designed to stimulate the biofilm growth.

The bacteria in the slime-inducing growth medium on the right side produced biofilm, but not uniformly. Instead the researchers observed a gradient: the cultures toward the middle of the plate, nearest to the left-side bacteria feasting on the nutrient-rich medium, oozed the most slime and took on a pinkish tint. Those cultures farthest from the well-fed bacteria on the rightmost side of the plate were least slimy and least pink. Because each bacterial colony grew in its own individual well, with no direct contact between colonies, the researchers suspected that the slimy colonies on the right side of the plate were somehow responding to airborne signals from the well-fed colonies on the left. Detection of such airborne signals would explain the slime gradient, because compared with the rightmost colonies, the slimy right-side colonies closest to the middle of the plate would detect more of the molecules floating over from the colonies on the left.

"The only thing that could cause this was something produced by bacteria in nutrient-rich medium—and it had to be produced as something in the air because there was no other medium connecting them," says Reindert Nijland, a marine biologist at Newcastle University and lead author of the new study.

The experimenters tested whether they could replicate the slime gradient in other kinds of bacteria, including Bacillus subtilis, Micrococcus luteus and Escherichia coli. Each time they found the same effect: the closer a nutrient-deprived colony grew to bacteria in a nutrient-rich medium, the slimier the former got. "We tested a whole bunch of strains we had in the lab, isolated from seaweed, crabs and sharks," Nijland says. "I found that it didn't matter which strain of bacteria we used as long as I was using the rich medium that contained a lot of ammonia."

Whenever the researchers grew bacterial colonies in a medium containing ammonia sulfate—which many bacteria break down into ammonia to acquire nitrogen—neighboring colonies in different media responded by producing greater amounts of slime. Noting this, the experimenters deduced that ammonia was the airborne molecule to which the bacteria were responding. Nijland thinks that when the well-fed bacteria broke down the nutrients in their growth medium and emitted excess ammonia as a metabolic by-product, neighboring colonies detected the gas and responded by producing biofilm. To further confirm their results, the researchers grew bacterial colonies near wells filled with a solution of ammonia and found the same slime gradient. Again and again, the bacterial colonies oozed slime in response to ammonia.

One possibility is that the bacteria were not actually responding to the presence of neighboring colonies, but were simply producing biofilm because ammonia raised the pH of the bacteria's surroundings—an environmental stressor that could encourage slimy growth. The researchers note, however, that they observed their results even with low ammonia concentrations that did not significantly alter pH; they also buffered the growth media to further control for changes in pH.

The researchers concluded that bacteria are capable of olfaction—the biological detection of volatile chemicals across a distance—and hypothesize that this sense may have first evolved in bacteria. Although the researchers are not sure how bacteria detect airborne ammonia, they have some hypotheses about why bacteria produce slime in response to volatile ammonia. "They sense this ammonia, and this is an indication for them of nutrients nearby," Nijland says, explaining that airborne ammonia could clue in bacterial colonies not only to the location of vital resources, but also to rival colonies that have already accessed those resources. Biofilm, the researchers think, could serve a dual function: It could help bacterial colonies grow toward resources as a collective swarm, and it might also help block out competing colonies.

"We've shown that bacteria can smell when food is nearby and respond to that," Nijland says. "I would be inclined to say it's more a way of accessing nutrients, but at the same time that means other bacteria are there already, so it would make sense to also switch on your defenses. Biofilm could be both a form of protection and a means of migration."

Oscar Kuipers, a molecular geneticist at the Groningen Biomolecular Sciences and Biotechnology Institute in the Netherlands whose work focuses on bacteria, is particularly interested in why bacteria would need to sense ammonia in the environment. He proposes that for bacteria living in a dry environment, where molecules could not easily diffuse between colonies, airborne ammonia could serve as an important indicator of nitrogen sources. Furthermore, Kuipers agrees that bacteria in dry environments could best reach these resources by spreading over land using biofilm. He also speculates that slime could protect bacteria from high levels of toxic gas.

Because biofilms increase bacteria's resistance to antibiotics and are known to coat many implanted medical devices, learning more about how and why bacteria produce slime could have important medical applications. "Pathogens tend to form thick biofilms in plastic catheters," Sperandio says, "and there's also a lot of cases in which heart valves are contaminated with biofilm, which can make patients septicemic [infected]. Biofilms are hard to control by the nature of the beasts."

"I think the next thing they have to do is find the bacterial sensor for ammonia," Sperandio adds. Kuipers agrees. "Interestingly, the volatile has to be sensed in some way, perhaps via a receptor or transport system, and the signal needs to be passed on to induce the genes responsible for biofilm formation," he wrote via e-mail. "A big challenge is to find out how this signal transduction takes place at the molecular level."

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