TY - JOUR
T1 - Outer membrane permeability of cyanobacterium Synechocystis sp. strain PCC 6803
T2 - Studies of passive diffusion of small organic nutrients reveal the absence of classical porins and intrinsically low permeability
AU - Kowata, Hikaru
AU - Tochigi, Saeko
AU - Takahashi, Hideyuki
AU - Kojima, Seiji
N1 - Funding Information:
This work was supported by a JSPS Grant-in Aid for Young Scientists (B) (grant 15K20860) to S.K. and JSPS Grant-in-Aid for JSPS Research Fellow (grant 17J03811) to H.K.
PY - 2017
Y1 - 2017
N2 - The outer membrane of heterotrophic Gram-negative bacteria plays the role of a selective permeability barrier that prevents the influx of toxic compounds while allowing the nonspecific passage of small hydrophilic nutrients through porin channels. Compared with heterotrophic Gram-negative bacteria, the outer membrane properties of cyanobacteria, which are Gram-negative photoautotrophs, are not clearly understood. In this study, using small carbohydrates, amino acids, and inorganic ions as permeation probes, we determined the outer membrane permeability of Synechocystis sp. strain PCC 6803 in intact cells and in proteoliposomes reconstituted with outer membrane proteins. The permeability of this cyanobacterium was >20-fold lower than that of Escherichia coli. The predominant outer membrane proteins Slr1841, Slr1908, and Slr0042 were not permeable to organic nutrients and allowed only the passage of inorganic ions. Only the less abundant outer membrane protein Slr1270, a homolog of the E. coli export channel TolC, was permeable to organic solutes. The activity of Slr1270 as a channel was verified in a recombinant Slr1270-producing E. coli outer membrane. The lack of putative porins and the low outer membrane permeability appear to suit the cyanobacterial autotrophic lifestyle; the highly impermeable outer membrane would be advantageous to cellular survival by protecting the cell from toxic compounds, especially when the cellular physiology is not dependent on the uptake of organic nutrients.
AB - The outer membrane of heterotrophic Gram-negative bacteria plays the role of a selective permeability barrier that prevents the influx of toxic compounds while allowing the nonspecific passage of small hydrophilic nutrients through porin channels. Compared with heterotrophic Gram-negative bacteria, the outer membrane properties of cyanobacteria, which are Gram-negative photoautotrophs, are not clearly understood. In this study, using small carbohydrates, amino acids, and inorganic ions as permeation probes, we determined the outer membrane permeability of Synechocystis sp. strain PCC 6803 in intact cells and in proteoliposomes reconstituted with outer membrane proteins. The permeability of this cyanobacterium was >20-fold lower than that of Escherichia coli. The predominant outer membrane proteins Slr1841, Slr1908, and Slr0042 were not permeable to organic nutrients and allowed only the passage of inorganic ions. Only the less abundant outer membrane protein Slr1270, a homolog of the E. coli export channel TolC, was permeable to organic solutes. The activity of Slr1270 as a channel was verified in a recombinant Slr1270-producing E. coli outer membrane. The lack of putative porins and the low outer membrane permeability appear to suit the cyanobacterial autotrophic lifestyle; the highly impermeable outer membrane would be advantageous to cellular survival by protecting the cell from toxic compounds, especially when the cellular physiology is not dependent on the uptake of organic nutrients.
KW - Cyanobacteria
KW - Gram-negative bacteria
KW - Outer membrane
KW - Permeability
KW - Porins
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U2 - 10.1128/JB.00371-17
DO - 10.1128/JB.00371-17
M3 - Article
C2 - 28696278
AN - SCOPUS:85028845369
VL - 199
JO - Journal of Bacteriology
JF - Journal of Bacteriology
SN - 0021-9193
IS - 19
M1 - e00371-17
ER -