Mechanosensitive channel functions to alleviate the cell lysis of marine bacterium, <i>Vibrio alginolyticus</i>, by osmotic downshock

Nakamaru, Yoshinobu; Takahashi, Yuuichirou; Unemoto, Tsutomu; Nakamura, Tatsunosuke

doi:10.1016/s0014-5793(99)00054-x

Cited by 42 publications

(25 citation statements)

References 14 publications

(20 reference statements)

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“…Vibrio alginolyticus grows in marine environments and lyses when transferred to low osmolarity. Lysis can be prevented by expressing E. coli MscL from a plasmid (62). The genome of this organism, along with those for many other Vibrio species, has subsequently been sequenced.…”

Section: The Challenge Of Hypoosmotic Shockmentioning

confidence: 99%

The MscS and MscL Families of Mechanosensitive Channels Act as Microbial Emergency Release Valves

2012

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bSingle-celled organisms must survive exposure to environmental extremes. Perhaps one of the most variable and potentially lifethreatening changes that can occur is that of a rapid and acute decrease in external osmolarity. This easily translates into several atmospheres of additional pressure that can build up within the cell. Without a protective mechanism against such pressures, the cell will lyse. Hence, most microbes appear to possess members of one or both families of bacterial mechanosensitive channels, MscS and MscL, which can act as biological emergency release valves that allow cytoplasmic solutes to be jettisoned rapidly from the cell. While this is undoubtedly a function of these proteins, the discovery of the presence of MscS homologues in plant organelles and MscL in fungus and mycoplasma genomes may complicate this simplistic interpretation of the physiology underlying these proteins. Here we compare and contrast these two mechanosensitive channel families, discuss their potential physiological roles, and review some of the most relevant data that underlie the current models for their structure and function.

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Section: The Challenge Of Hypoosmotic Shockmentioning

confidence: 99%

The MscS and MscL Families of Mechanosensitive Channels Act as Microbial Emergency Release Valves

2012

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“…Such apparent biochemical redundancy implied that observation of a phenotype might require the construction of a mutant lacking more than one channel protein. Preliminary support for the protective role of MscL was discovered by expressing the channel in Vibrio and observing protection from hypoosmotic shock (38). The discovery of the structural gene for MscS, the second major MS channel in E. coli, allowed this functional hypothesis to be tested (25).…”

Section: Overview Of Key Developmentsmentioning

confidence: 99%

Two Families of Mechanosensitive Channel Proteins

Pivetti

Yen

Miller

et al. 2003

Microbiol Mol Biol Rev

216

222

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Mechanosensitive (MS) channels were first demonstrated in bacterial cells by using patch clamp analysis of giant bacterial protoplasts and by fusion of membranes with liposomes. Both approaches indicated the presence of high-conductance channels in the membranes of gram-positive and gram-negative bacteria (15,29,53,60). Initially the data were greeted with scepticism, based on the similarity of the conductances of MS channels to those of porins and the recognized need of the cytoplasmic membrane to exhibit tight control over H ϩ permeability in order to effect energy transduction. Activation of MS channels by membrane-intercalating amphipathic compounds suggested that these channels are sensitive to mechanical perturbations in the lipid bilayer (22,28). Support for the presence of channels was provided by the discovery and reconstitution of two distinct channel activities from Escherichia coli, each with unique properties (52). Further support came from the discovery that the efflux of solutes from E. coli cells in response to a lowering of the external osmolarity could be prevented by gadolinium ions, which are classical inhibitors of MS channels in higher organisms (6).A landmark event was the purification and cloning of the first MS channel protein, MscL, from E. coli. This heroic piece of biochemistry required that each fraction derived from the solubilized and fractionated membrane be reconstituted into liposomes and the MS channel activity be measured (51). Availability of the amino-terminal sequence of the protein led to identification of the gene. Following this breakthrough, a new age of MS channel protein structure-function analysis dawned (7,(9)(10)(11)42), culminating in the crystal structure of a mycobacterial MscL channel (13) (Fig. 1). Extensive genetic and biophysical analyses of MscL protein movement in real time, coupled with model building, electron paramagnetic resonance spectroscopy, and site-directed spin labeling studies, provided an explanation of how the protein can exist in at least two states-one tightly closed and the other creating a large pore in the membrane (23,42,48,49) (Fig. 2). MS channels are now thought to be important to many bacteria (8) and archaea (20,21,24).The genetic advances with MscL posed a further problemwhy does an mscL null mutant lack an apparent physiological phenotype? Patch clamp analysis had revealed the presence of at least two MS channels in E. coli membranes, and subsequent studies led to the possibility that five or more genetically distinct channels exist (5). Such apparent biochemical redundancy implied that observation of a phenotype might require the construction of a mutant lacking more than one channel protein. Preliminary support for the protective role of MscL was discovered by expressing the channel in Vibrio and observing protection from hypoosmotic shock (38). The discovery of the structural gene for MscS, the second major MS channel in E. coli, allowed this functional hypothesis to be tested (25). Through the genetic analysis of a missense mu...

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“…Subsequent genetic experiments with the marine bacterium Vibrio alginolyticus revealed that the introduction of this gene alleviates cell lysis following osmotic downshock (17). Similar functions were also demonstrated in the Gram-positive bacteria Lactococcus lactis (7) and Bacillus subtilis (8).…”

mentioning

confidence: 71%

“…While the genetic basis for the failure of Salinispora strains to grow in low-osmotic-strength media has not been established, comparative genomics revealed a large family of highly duplicated polymorphic membrane proteins (PMPs), which were proposed to render cells unable to survive osmotic downshock (19). A more comprehensive bioinformatic analysis identified a larger pool of candidate marine adaptation genes and the lineage-specific loss of mscL (20), the product of which is a mechanosensitive channel that has been shown to alleviate cell lysis following osmotic downshock (17).…”

mentioning

confidence: 99%

Genetic Complementation of the Obligate Marine Actinobacterium Salinispora tropica with the Large Mechanosensitive Channel Gene mscL Rescues Cells from Osmotic Downshock

Bucarey

Penn

Paul

et al. 2012

Appl Environ Microbiol

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ABSTRACTMarine actinomycetes in the genusSalinisporafail to grow when seawater is replaced with deionized (DI) water in complex growth media. While bioinformatic analyses have led to the identification of a number of candidate marine adaptation genes, there is currently no experimental evidence to support the genetic basis for the osmotic requirements associated with this taxon. One hypothesis is that the lineage-specific loss ofmscLis responsible for the failure of strains to grow in media prepared with DI water. ThemscLgene encodes a conserved transmembrane protein that reduces turgor pressure under conditions of acute osmotic downshock. In the present study, themscLgene from aMicromonosporastrain capable of growth on media prepared with DI water was transformed intoS. tropicastrain CNB-440. The single-copy, chromosomal genetic complementation yielded a recombinantSalinispora mscL+strain that demonstrated an increased capacity to survive osmotic downshock. The enhanced survival of theS. tropicatransformant provides experimental evidence that the loss ofmscLis associated with the failure ofSalinisporaspp. to grow in low-osmotic-strength media.

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Mechanosensitive channel functions to alleviate the cell lysis of marine bacterium, Vibrio alginolyticus, by osmotic downshock

Cited by 42 publications

References 14 publications

The MscS and MscL Families of Mechanosensitive Channels Act as Microbial Emergency Release Valves

The MscS and MscL Families of Mechanosensitive Channels Act as Microbial Emergency Release Valves

Two Families of Mechanosensitive Channel Proteins

Genetic Complementation of the Obligate Marine Actinobacterium Salinispora tropica with the Large Mechanosensitive Channel Gene mscL Rescues Cells from Osmotic Downshock

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