Revealed fragility of extremophiles bacteria

Most living (micro)organisms are adapted to life at room temperature. Bacteria that thrive in these conditions are called mesophiles. But evolution has also enabled certain bacteria to live only in extreme conditions, particularly in terms of temperature. This is the case for hyperthermophilic bacteria, which are capable of surviving at temperatures above 100°C. Conversely, psychrophilic bacteria only survive at low temperatures, well below 0°C.

In these single-celled microorganisms known as bacteria, as well as in each individual cell of a living organism, the way proteins move in the highly populated environment of the cytoplasm reveals the state of health of microscopic life. Cellular life depends on a delicate balance between the structure and mobility of proteins (and enzymes) that ensure the vital reactions of cellular metabolism. In the model bacterium Escherichia coli, recent work has shown that as the fatal temperature that causes cell death approaches, proteins slow down abruptly: a small fraction of them begin to unfold. The unfolded proteins become entangled and transform the cytoplasm into a kind of highly viscous gel. This change in structure is accompanied by a loss of functionality and cell death [1].

But is this scenario universal? In other words, what about bacteria adapted to living conditions at extreme temperatures? To find out, a Franco-Italian team of scientists compared three bacteria adapted to opposite thermal environments: Psychrobacter arcticus (P. arcticus, psychrophile), Escherichia coli (E. coli, mesophile) and Aquifex aeolicus (A. aeolicus, hyperthermophile). Molecular simulations combined with neutron scattering experiments enabled them to track the collective movement of proteins within these three types of cells as a function of temperature.

The study shows that, in all three cases, the sudden loss of protein mobility in the cytoplasm is indeed caused by their gradual unfolding. A few unfolded proteins are enough to create a tangled network of these macromolecules, greatly increasing the viscosity of the cytoplasm. However, in the cold-adapted bacterium, a surprising result was obtained: the cell dies about 20°C before this global unfolding of proteins begins. In other words, the proteins remain structured and mobile even though metabolism has already stopped. This death well before the proteins become unstructured overturns one of the key ideas in biology, namely that protein stability automatically guarantees cell survival. In cold-adapted organisms, the extreme flexibility required to function at low temperatures makes vital processes very sensitive to even the slightest warming. Enzymes cease to function without unfolding, and the cell collapses without any visible signs of structural degradation.

These results, published in the journal Nature Communications, show that perfect adaptation to cold comes at a price: high thermal sensitivity and fragility. They open up new avenues for understanding the limits of life and the evolution of extremophiles, but also for exploiting or protecting these organisms in a warming world.

[1] D. Di Bari, S. Timr, M. Guiral, M.T. Giudici-Orticoni, T. Seydel, C. Beck, C. Petrillo, P. Derreumaux, S. Melchionna, F. Sterpone, J. Peters, A. Paciaroni, Diffusive Dynamics of Bacterial Proteome as a Proxy of Cell Death, ACS Cent Sci 9(1) (2023) 93–102.