Mechanosensitive Channels in Prokaryotes

Abstract

Compared to voltage-dependent or ligand-gated ion channels that have extensively been studied over the last twenty years, there is little knowledge available on structure and function of mechanosensitive (MS) channels that constitute the third major group of ion channels classified according to their gating mechanism. The main purpose of this review is to summarize an area of the MS channel research where major progress has occurred. Cloning of MscL and MscS, the MS channels of Large and Small conductance found in Bacteria and elucidation of the 3D crystal structure of MscL are discussed in conjunction with the physiological role of the MS channels in bacterial osmoregulation. Furthermore, cloning and molecular characterization of MS channels in Archaea Methanococcus jannashii and Thermoplasma acidophilum are described. They present examples of the recent promising developments, which may ultimately lead to the understanding of the biophysical principles and evolutionary origins of mechanosensory transduction. Although they conduct ions and are usually characterized by their ionic conductance and selectivity, the MS channels in prokaryotes may primarily serve to transport osmoticants other than ions. Therefore, throughout this review prokaryotic MS ion channels are referred to as MS channels rather than MS ion channels.

How did cells get their size?

“…Returning to this theme and elaborating, we should consider whether very early integral membrane peptides might have formed pores that served as crude osmotic valves. Today's prokaryotes have nonselective highthroughput channels that open with extreme osmotic stress (Martinac, 2001). In feedback terms, these are sensor/effector proteins that detect/relieve osmotic stress.…”

“…Modern prokaryote osmotic valves are self-assembling pentamers whose N-termini are thought to hinge to form the channel's gate Martinac, 2001). Detailed kinetic analyses suggest that 1) the gate is not tightly coupled to the in-plane area change during the channel's initial expansion phase, and 2) the bilayer-embedded pore region of the channel expands by ϳ20 nm 2 in the plane of the bilayer, mostly before the gate begins to open .…”

“…One open MscL channel per bacterium would suffice for near instantaneous dumping of all osmolytes, yet bacteria make many copies, as well as multiple copies of related channels (Martinac, 2001). Unstimulated (thermal) MscL channel openings would cost a bacterium precious solutes (e.g., nucleotide bases and ATP), so why risk having many when only one is needed?…”

Structural Rearrangements of MscS during Activation Gating

“…The molecular basis for mechanosensation requires the understanding of the energy transduction that converts the stimuli into cell response; in most of the systems this conversion occurs through mechanosensitive ion channels. It has been suggested that they might have evolved as cellular osmoregulators that sensed small changes in the concentration of water across membranes of primitive cells such as bacteria (Batiza et al, 1999;Blount, 2003;Hamill and Martinac, 2001;Kung, 2005;Martinac, 2001Martinac, , 2004Perozo, 2006).…”

“…The global pattern of mobilities and accessibilities were used to refine the x-ray structure to build a three-dimensional model of MscS in the closed state, which had significant differences with the crystal structure of MscS obtained in a detergent micelle. suggested that mechanosensitive channels might have evolved as cellular osmoregulators that sensed changes in the concentration of water across bacteria membranes (Batiza et al, 1999;Blount, 2003;Hamill and Martinac, 2001;Kung, 2005;Martinac, 2001Martinac, , 2004Perozo, 2006). Mechanosensitive channels belong to a structurally heterogeneous group, and have been classified according to their function rather than topology.…”