The Bacterial Cytoplasm Has Glass-like Properties and Is Fluidized by Metabolic Activity

Abstract

SUMMARY The physical nature of the bacterial cytoplasm is poorly understood even though it determines cytoplasmic dynamics and hence cellular physiology and behavior. Through single-particle tracking of protein filaments, plasmids, storage granules and foreign particles of different sizes, we find that the bacterial cytoplasm displays properties characteristic of glass-forming liquids and changes from liquid-like to solid-like in a component size-dependent fashion. As a result, the motion of cytoplasmic components becomes disproportionally constrained with increasing size. Remarkably, cellular metabolism fluidizes the cytoplasm, allowing larger components to escape their local environment and explore larger regions of the cytoplasm. Consequently, cytoplasmic fluidity and dynamics dramatically change as cells shift between metabolically active and dormant states in response to fluctuating environments. Our findings provide insight into bacterial dormancy and have broad implications to our understanding of bacterial physiology as the glassy behavior of the cytoplasm impacts all intracellular processes involving large components.

Molecular simulations of cellular processes

“…This view, consistent with experiments (Weber et al 2010;Parry et al 2014), is confirmed by the calculated anomalous exponents α. While small biomolecules diffuse almost normally, crowders with sizes between 100 and 800 Å show anomalous diffusion with α ranging between 0.75 and 0.85 over 350 μs of simulation.…”

“…Hence, they determine the macroscopic properties of the cytoplasm both in physiological conditions and under stress (Parry et al 2014;Joyner et al 2016;Munder et al 2016). These and the previous examples are clear evidence of the importance of chemical interactions between macromolecules, despite their weak strength, and suggest that they are as relevant as the specific interactions responsible for biomolecule folding and complex formation.…”

Osmotaxis in Escherichia coli through changes in motor speed

“…For example, previous observations indicate that at higher external osmolarities, osmotic pressure is kept the same [Pilizota and Shaevitz, 2014]. Thus, the crowding in an already crowded cytoplasm [Parry et al, 2014] increases, which can affect cytoplasmic interactions [Klumpp et al, 2013, Paudel andRueda, 2014] and the binding of CheY-P to the BFM, perhaps in a similar fashion to that observed at higher hydrostatic pressures [Nishiyama et al, 2013]. However, it is also possible that the observed changes in τ CCW and ω are a consequence of signal processing by the chemotactic network.…”

Bacterial Inclusion Bodies: Discovering Their Better Half

“…To transform the cytoplasm from a glassy (macromolecular crowded) to a more fluidic environment allowing movement of larger particles (>30 nm) requires ATP-hydrolysis and active metabolism [18,19]. Thus, it is possible that IB formation occurs passively but only when biochemical reactions and active metabolism are disturbing the glassy structure of the cytoplasm.…”