Bacterial spores survive extreme environmental conditions and, in their apparently lifeless state, appear to be unaware of the outside world. Nevertheless, they can perceive positive environmental stimuli and, under favorable conditions, germinate again within a short time. A study now shows how this is possible: According to this, the bacterial spores use a stored electrochemical potential that slowly decreases in response to repeated positive stimuli until a threshold value is reached that triggers germination. This passive mechanism enables seemingly lifeless organisms to process information from the environment that is relevant to them.
Faced with hunger and stress, some bacteria enter a dormant state where their life processes come to a halt. As spores, this allows them to withstand extreme conditions of heat and pressure, and even the harsh conditions of outer space. When conditions are favourable, spores that have been dormant for years can come back to life in minutes: they re-absorb water and their metabolism kicks in. But how do the seemingly lifeless, dormant spores find out when conditions are favorable again?
Germination only after repeated impulses
A team led by Kaito Kikuchi from the University of California in San Diego has now uncovered this mystery. The researchers placed a special focus on the question of how bacterial spores process vague environmental signals that do not indicate clearly favorable conditions. Previous observations had suggested that the bacterial spores can mysteriously remember a history of weakly positive environmental conditions - and are more likely to germinate with repeated weakly positive signals than with just one such impulse. But how is that possible if no metabolic processes are taking place?
Kikushi and his team conducted experiments on thousands of hay bacillus (Bacillus subtilis) spores. First, they added a small amount of nutrients to the spores, which are known to stimulate germination. However, since the amount was so small and only present for a short time, 95 percent of the spores remained dormant after this first pulse. However, if the researchers added a small amount of nutrients two hours later, around half of all the spores germinated. "The spores are thus sensitized by the first exposure and appear to be approaching a germ threshold," the researchers explain. Physiologically, this can make sense, as it allows the bacteria to assess whether the conditions are actually good enough for germination and not be tempted by temporary positive signals to leave their dormant state too soon.
Signal processing via membrane potential
Measurements of the membrane potential of the spores revealed how Bacillus subtilis is able to register and store the information: every small impulse to germinate caused the membrane potential to drop a little. "We discovered that spores can release their energy stored in the form of an electrochemical membrane potential to perform calculations about their environment without the need for metabolic activity," explains Kikushi's colleague Gürol Süel. "It changes the way we think about spores, which were previously thought of as unresponsive objects."
When the bacteria go into the spore state in poor environmental conditions, they store positively charged potassium ions inside them. This creates an electrochemical potential at the cell membrane. When the spores receive a stimulus to germinate, some of the potassium ions passively leak out of the cell through ion channels, causing the electrochemical potential across the membrane to drop. If the impulse is so low that only a small part of the potassium ions escapes, this is not enough to trigger germination. However, as multiple pulses accumulate, the membrane potential eventually reaches a threshold. A small impulse is then sufficient for the cell to leave its resting state.
"The way spores process information is similar to how neurons in our brain work," explains Süel. “In both bacteria and neurons, small and short inputs are summed 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.” The researchers represented this mechanism, also known as “integrating and firing”, in a mathematical model – and they were actually able to they use it to explain the behavior of the bacterial spores.
Further details still open
It is still unclear what exactly causes the potassium ions to flow out of the cell. The question of why and how a changed membrane potential causes the cell to come back to life is also still an open question. "Future work examining the germination behavior of spores from different taxa could provide useful insights into how environmental conditions dictate germination thresholds," write Jonathan Lombardino and Briana Burton of the University of Wisconsin-Madison in a commentary accompanying the study. also published in the journal Science.
But the results so far already have far-reaching implications: "This work shows alternative ways to deal with the potential threat of pathogenic spores and has implications for what we can expect from extraterrestrial life," said Süel. "When scientists find life on Mars or Venus, it is likely in a dormant state, and we now know that a life form that appears completely unresponsive may still be able to contemplate its next moves. "
Source: Kaito Kikuchi (University of California at San Diego) et al., Science, doi: 10.1126/science.abl7484