bacterial intelligence: stress responses (Animals)

by David Turell , Friday, November 25, 2022, 16:30 (509 days ago) @ David Turell

Research described in a prize essay:

https://www.sciencemagazinedigital.org/sciencemagazine/library/item/25_november_2022/40...

A key to the impressive success of bacteria in nature is their ability to adapt to new environments. Owing to their short generation times, these adaptations often result from genetic evolution. For instance, bacteria can rapidly evolve to acquire drug resistance or to specialize in the consumption of a resource. Environmental fluctuations, however, can also happen at much shorter time scales that preclude adaptation by genetic mutation.

Bacteria have sophisticated programs of gene regulation that control decisions involving hundreds of genes and lead to major physiological changes (e.g., the ability to become a dormant spore in unfavorable conditions). Bacteria rely on their ability to sense the environment to make these decisions, yet the information that one individual bacterium can gather is often incomplete or noisy. I found that bacteria can solve this problem when they sense the environment as a collective by quorum sensing (QS)—a process in which they secrete and respond to small molecules in the extracellular environment known as autoinducers.

The established view of QS is that bacteria use autoinducers to measure population density to control the expression of traits that require coordination and are only beneficial when expressed by many cells (e.g., bioluminescence). However, we found that beyond coordination of group behavior, QS could be used by bacteria to collectively sense their environment. The seed of this idea came from studying Streptococcus pneumoniae, a species that inhabits the nasopharynx and is a leading cause of pneumonia. S. pneumoniae uses QS to control the entry into competence: a state in which it up-regulates the expression of stress response genes together with machinery to take up and integrate extracellular DNA into its own genetic material.

I [found] that although competence is regulated by population density, it simultaneously responds to various environmental factors including pH and antibiotics. This joint regulation occurs because bacteria do not secrete autoinducers at a constant rate but instead modulate this rate dependent on the environment they encounter. For instance, upon exposure to a DNA-damaging agent, S. pneumoniae strongly up-regulates the secretion of autoinducers, and competence develops even when the quorum is low. This process helps bacteria fight off DNA damage through the uptake of extracellular genetic material in the competent state.

***

I found that bacteria profit from QS because autoinducer secretion allows them to pool their imperfect estimates of the environment and average out individual noise. Then, as they monitor the extracellular concentration of autoinducers, bacteria improve their estimation accuracy and make betterinformed decisions about how to respond to the environment. In other words, bacteria exploit a well-known principle in decision theory: the wisdom of crowds.

***

Bacteria are often studied in the laboratory when they are actively growing, yet most bacteria in nature are in starved states where they eagerly await their next meal. To immediately resume growth when resources become available may seem like the best strategy for a bacterium because it maximizes its number of descendants. However, rapid resumption of growth makes bacteria vulnerable to several stressors that act primarily on dividing cells. Without any cues to anticipate whether stress is on the horizon, how can bacteria resolve this trade-off between growth and survival?

***

I developed a device to follow the behavior of populations of Escherichia coli as they resume growth from starvation. Microscopy was used to observe hundreds of cells while they undergo this transition, and I found that there is large variation in lag time between populations of genetically identical bacteria. Whereas some individuals resumed growth right away, others of their clonemates took over 20 generations more to start reproducing

This variation is not optimal for growth. Indeed, bacteria selected to resume rapid growth in stress-free conditions evolved shorter and less varied lag times than wildtype E. coli. However, this variation might be beneficial in times of stress...As a result, populations of mutants that evolved narrow lag time distributions—in which all bacteria began growing immediately—were fully eliminated by antibiotics, whereas wild-type populations with a mix of dormant and growing bacteria could survive.

***

With mathematical modeling, I showed that intermittent exposure to antibiotics during feast-to-famine cycles can lead to the evolution of genotypes that have wide lag time distributions.

***

Bacteria are one of the simplest forms of life on Earth. Despite their apparent simplicity, they deploy a variety of strategies to thrive in fluctuating environments. From relying on a hive mind, to hedging their bets like seasoned investors, or rapidly adapting by genetic mutation, bacteria seem to have figured out that the best way to cope with change is to play every possible trick in the book.

Comment: Bacteria, as single cell, must have these abilities to survive. As they were the first life, they must have had them when they first appeared. Obviously designed this way.