Unexpected bacterial cell activity provides insights about life in extreme states on Earth and maybe on other worlds.
Some bacteria go into a dormant state where their life processes cease when they face starvation and stressful conditions. These cells, known as spores, can resist punishing extremes of heat, pressure, and even the harsh environment of space by entering a deep dormancy.
When the right circumstances arise, spores that may have been dormant for years may eventually awaken and spring back to life within minutes.
Spores awaken by rehydrating and restarting their metabolism and physiology. But up until this point, scientists were unsure whether spores could monitor their surroundings while still “in their sleep” without waking up. It was unknown, in particular, how spores respond with ambiguous environmental signals that do not indicate clearly favorable conditions. Would spores just disregard such mixed conditions or take note?
Biologists from the University of California, San Diego have solved this mystery in a recent study that was published in the journal Science. Researchers from the School of Biological Sciences revealed that spores had an extraordinary ability to evaluate their surroundings despite remaining physiologically dead. They discovered that spores employ stored electrochemical energy to detect if conditions are suitable for a return to normal functioning life, much like a capacitor.
“This work changes the way we think about spores, which were considered to be inert objects,” said Gürol Süel, a professor in the Department of Molecular Biology. “We show that cells in a deeply dormant state have the ability to process information. We discovered that spores can release their stored electrochemical potential energy to perform a computation about their environment without the need for metabolic activity.”
A microscopy time-lapse movie depicts the color-coded electrochemical potential value overlaid on top of the phase image of a single spore. As revealed by the phase image, the spore remains dormant while exhibiting the ability to count stimuli, as indicated by the multicolor-coded flashes of electrochemical potential changes. Credit: Süel Lab—Kaito Kikuchi
Many bacterial species form spores—partially dehydrated cells surrounded by a resilient protective coat—as a survival strategy that allows them to remain dormant for thousands of years. Such a remarkable capability makes them a threat in the form of bacterial anthrax as well as a contamination hazard in medicine and the food industry.
Süel and his colleagues tested whether dormant Bacillus subtilis spores could sense short-lived environmental signals that were not strong enough to trigger a return to life. They found that spores were able to count such small inputs and if the sum reached a certain threshold, they would decide to exit the dormant state and resume biological activity.
This microscopy time-lapse movie shows the color-coded jumps in the electrochemical potential value of a single spore in response to short stimuli. With each stimulus, the spore gets closer and closer to exiting dormancy, as visualized by the color transitioning from deep purple to yellow. Credit: Süel Lab—Kaito Kikuchi
Developing a mathematical model to help explain the process, the researchers discovered that spores use a mechanism known as integrate-and-fire, based on fluxes of potassium ions for appraising the surrounding environment. They found that spores responded to even short-lived favorable signals that were not enough to trigger an exit from dormancy. Instead of waking up, spores released some of their stored potassium in response to each small input and then summed consecutive favorable signals to determine if conditions were suitable for exiting. Such a cumulative signal processing strategy can reveal whether external conditions are indeed favorable, and prevents spores from “jumping the gun” into a world of unfavorable conditions.
“The way spores process information is similar to how neurons operate in our brain,” said Süel. “In both bacteria and neurons, small and short inputs are added up over time to determine if a threshold is reached. Upon reaching the threshold spores initiate their return to life, while neurons fire an action potential to communicate with other neurons.” Interestingly, spores can perform this signal integration without requiring any metabolic energy, while neurons are among the most energy-dependent cells in our bodies.
A composite movie showing the phase contrast of a single spore (top left) to visualize the dormant state. A movie (top right) shows the color-coded electrochemical potential of the same spore. The plot (bottom left) shows the corresponding time trace of the electrochemical potential values changing over time. Finally, a corresponding bar plot (bottom right) visualizes the jumps toward the threshold for returning to life. Credit: Süel Lab
The researchers believe the new information about spores reframes popular ideas about cells in extremely dormant states that seem dead. Such findings hold implications for evaluating life on objects such as meteors as well as space missions seeking evidence of life.
“This work suggests alternate ways to cope with the potential threat posed by pathogenic spores and has implications for what to expect from extraterrestrial life,” said Süel, who holds affiliations with the San Diego Center for Systems Biology, BioCircuits Institute and Center for Microbiome Innovation. “If scientists find life on Mars or Venus, it is likely to be in a dormant state and we now know that a life form that appears to be completely inert may still be capable of thinking about its next steps.”
Reference: “Electrochemical potential enables dormant spores to integrate environmental signals” by Kaito Kikuchi, Leticia Galera-Laporta, Colleen Weatherwax, Jamie Y. Lam, Eun Chae Moon, Emmanuel A. Theodorakis, Jordi Garcia-Ojalvo and Gürol M. Süel, 6 October 2022, Science.
The study was funded by the National Institute of General Medical Sciences, the Howard Hughes Medical Institute-Simons Foundation Faculty Scholars Program, the U.S. Army Research Office, the Defense Advanced Research Projects Agency, the Spanish Ministry of Science, the Innovation and Universities Project, FEDER, Generalitat de Catalunya ICREA Academia Programme, the ANRI Fellowship, and the National Institute on Aging.