DOI: 10.1126/science.3941890. Osmotic Adaptation by Gram-Negative Bacteria: Possible Role for Periplasmic Oligosaccharides

Osmotic Adaptation by Gram-Negative Bacteria: Possible Role for Periplasmic Oligosaccharides

10.1126/science.3941890

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The cyclic (1 → 2)-β-D-glucans produced by species of Agrobacterium and Rhizobium resemble the membrane-derived oligosaccharides of Escherichia coli in their periplasmic localization, intermediate size, and (1 → 2)-β-D-glucan backbones. The regulation of the biosynthesis of cyclic (1 → 2)-β-D-glucan by Agrobacterium tumefaciens is now shown to parallel the osmotic regulation of membrane-derived oligosaccharide biosynthesis in Escherichia coli . This result suggests a general role for periplasmic oligosaccharides in the osmotic adaptation of Gram-negative bacteria as ecologically diverse as enteric and soil bacteria.

Bibliography

Miller, K. J., Kennedy, E. P., & Reinhold, V. N. (1986). Osmotic Adaptation by Gram-Negative Bacteria: Possible Role for Periplasmic Oligosaccharides. Science, 231(4733), 48â51.

Authors 3

Karen J. Miller (first)
Eugene P. Kennedy (additional)
Vernon N. Reinhold (additional)

References 27 Referenced 221

ABE, M, STUDIES ON CYCLIC BETA-1,2-GLUCAN OBTAINED FROM PERIPLASMIC SPACE OF RHIZOBIUM-TRIFOLII CELLS, PLANT AND SOIL 64: 315 (1982). (10.1007/BF02372514) / PLANT AND SOIL (1982)
AMEMURA, A, CYCLIC (1-]2)-BETA-D-GLUCAN AND THE OCTASACCHARIDE REPEATING-UNITS OF EXTRACELLULAR ACIDIC POLYSACCHARIDES PRODUCED BY RHIZOBIUM, CARBOHYDRATE RESEARCH 114: 277 (1983). (10.1016/0008-6215(83)88194-4) / CARBOHYDRATE RESEARCH (1983)
BOHIN, J.P., MAPPING OF A LOCUS (MDOA) THAT AFFECTS THE BIOSYNTHESIS OF MEMBRANE-DERIVED OLIGOSACCHARIDES IN ESCHERICHIA-COLI, JOURNAL OF BACTERIOLOGY 157: 956 (1984). (10.1128/jb.157.3.956-957.1984) / JOURNAL OF BACTERIOLOGY (1984)
BOHIN, J.P., REGULATION OF THE SYNTHESIS OF MEMBRANE-DERIVED OLIGOSACCHARIDES IN ESCHERICHIA-COLI - ASSAY OF PHOSPHOGLYCEROL TRANSFERASE-I INVIVO, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 8388 (1984). (10.1016/S0021-9258(17)39742-9) / JOURNAL OF BIOLOGICAL CHEMISTRY (1984)
CSONKA, L.N., PROLINE OVER-PRODUCTION RESULTS IN ENHANCED OSMOTOLERANCE IN SALMONELLA-TYPHIMURIUM, MOLECULAR & GENERAL GENETICS 182: 82 (1981). (10.1007/BF00422771) / MOLECULAR & GENERAL GENETICS (1981)
DELL, A, HOST-SYMBIONT INTERACTIONS .14. THE CYCLIC STRUCTURE OF BETA-D-(1-]2)-LINKED D-GLUCANS SECRETED BY RHIZOBIA AND AGROBACTERIA, CARBOHYDRATE RESEARCH 117: 185 (1983). (10.1016/0008-6215(83)88086-0) / CARBOHYDRATE RESEARCH (1983)
EPSTEIN, E, GENETIC ENG OSMOREGU: 7 (1980). / GENETIC ENG OSMOREGU (1980)
HALL, M.N., GENETIC-ANALYSIS OF THE MAJOR OUTER-MEMBRANE PROTEINS OF ESCHERICHIA-COLI, ANNUAL REVIEW OF GENETICS 15: 91 (1981). (10.1146/annurev.ge.15.120181.000515) / ANNUAL REVIEW OF GENETICS (1981)
HANSON, R.S., MANUAL METHODS GEN B: 328 (1981). / MANUAL METHODS GEN B (1981)
HEPPEL, L.A., METHODS ENZYMOL B 12: 841 (1968). (10.1016/0076-6879(67)12200-3) / METHODS ENZYMOL B (1968)
HISAMATSU, M, STRUCTURAL STUDIES ON CYCLIC (1-]2)-BETA-D-GLUCANS (CYCLOSOPHORAOSES) PRODUCED BY AGROBACTERIUM AND RHIZOBIUM, CARBOHYDRATE RESEARCH 121: 31 (1983). (10.1016/0008-6215(83)84003-8) / CARBOHYDRATE RESEARCH (1983)
HISAMATSU, M, CYCLIC (1-]2)-BETA-D-GLUCAN AND THE OCTASACCHARIDE REPEATING-UNIT OF SUCCINOGLYCAN PRODUCED BY AGROBACTERIUM, JOURNAL OF GENERAL MICROBIOLOGY 128: 1873 (1982). / JOURNAL OF GENERAL MICROBIOLOGY (1982)
JEFFERIES, R.L., GENETIC ENG OSMOREGU: 135 (1980). / GENETIC ENG OSMOREGU (1980)
KENNEDY, E.P., IDENTIFICATION OF SN-GLYCERO-1-PHOSPHATE AND PHOSPHOETHANOLAMINE RESIDUES LINKED TO MEMBRANE-DERIVED OLIGOSACCHARIDES OF ESCHERICHIA-COLI, JOURNAL OF BIOLOGICAL CHEMISTRY 251: 4208 (1976). (10.1016/S0021-9258(17)33282-9) / JOURNAL OF BIOLOGICAL CHEMISTRY (1976)
KENNEDY, E.P., OSMOTIC REGULATION AND THE BIOSYNTHESIS OF MEMBRANE-DERIVED OLIGOSACCHARIDES IN ESCHERICHIA-COLI, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 1092 (1982). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1982)
KOIZUMI, K, SEPARATION OF CYCLIC (1-]2)-BETA-D-GLUCANS (CYCLOSOPHORAOSES) PRODUCED BY AGROBACTERIUM AND RHIZOBIUM, AND DETERMINATION OF THEIR DEGREE OF POLYMERIZATION BY HIGH-PERFORMANCE LIQUID-CHROMATOGRAPHY, JOURNAL OF CHROMATOGRAPHY 265: 89 (1983). (10.1016/S0021-9673(01)96701-9) / JOURNAL OF CHROMATOGRAPHY (1983)
LAIMINS, L.A., OSMOTIC CONTROL OF KDP OPERON EXPRESSION IN ESCHERICHIA-COLI, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 78: 464 (1981). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1981)
LERUDULIER, D, MOLECULAR-BIOLOGY OF OSMOREGULATION, SCIENCE 224: 1064 (1984). (10.1126/science.224.4653.1064) / SCIENCE (1984)
NIKAIDO, H, MOLECULAR-BASIS OF BACTERIAL OUTER-MEMBRANE PERMEABILITY, MICROBIOLOGICAL REVIEWS 49: 1 (1985). (10.1128/mr.49.1.1-32.1985) / MICROBIOLOGICAL REVIEWS (1985)
REINHOLD, V.N., NEW TECHNIQUES FOR OLIGOSACCHARIDE SEQUENCING, JOURNAL OF CARBOHYDRATE CHEMISTRY 2: 1 (1983). (10.1080/07328308308058806) / JOURNAL OF CARBOHYDRATE CHEMISTRY (1983)
SANFORD, P.A., BIOCHEM 5: 1508 (1966). (10.1021/bi00869a009) / BIOCHEM (1966)
SCHNEIDER, J.E., STRUCTURAL STUDIES OF THE MEMBRANE-DERIVED OLIGOSACCHARIDES OF ESCHERICHIA-COLI, JOURNAL OF BIOLOGICAL CHEMISTRY 254: 10135 (1979). (10.1016/S0021-9258(19)86683-8) / JOURNAL OF BIOLOGICAL CHEMISTRY (1979)
STOCK, J.B., PERIPLASMIC SPACE IN SALMONELLA-TYPHIMURIUM AND ESCHERICHIA-COLI, JOURNAL OF BIOLOGICAL CHEMISTRY 252: 7850 (1977). (10.1016/S0021-9258(17)41044-1) / JOURNAL OF BIOLOGICAL CHEMISTRY (1977)
VANLANGENHOVE, A, DETERMINATION OF POLYSACCHARIDE LINKAGE AND BRANCHING BY REDUCTIVE DEPOLYMERIZATION - GAS-LIQUID CHROMATOGRAPHY AND GAS-LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY REFERENCE DATA, CARBOHYDRATE RESEARCH 143: 1 (1985). (10.1016/S0008-6215(00)90691-8) / CARBOHYDRATE RESEARCH (1985)
YORK, W.S., BETA-2-LINKED GLUCANS SECRETED BY FAST-GROWING SPECIES OF RHIZOBIUM, JOURNAL OF BACTERIOLOGY 142: 243 (1980). (10.1128/jb.142.1.243-248.1980) / JOURNAL OF BACTERIOLOGY (1980)
ZEVENHUIZEN, LPT, SURFACE CARBOHYDRATES OF RHIZOBIUM .1. BETA-1, 2-GLUCANS, ANTONIE VAN LEEUWENHOEK JOURNAL OF MICROBIOLOGY 45: 165 (1979). (10.1007/BF00418581) / ANTONIE VAN LEEUWENHOEK JOURNAL OF MICROBIOLOGY (1979)
ZEVENHUIZEN, LPT, CELLULAR GLYCOGEN, BETA-1,2-GLUCAN, POLY-BETA-HYDROXYBUTYRIC ACID AND EXTRACELLULAR POLYSACCHARIDES IN FAST-GROWING SPECIES OF RHIZOBIUM, ANTONIE VAN LEEUWENHOEK JOURNAL OF MICROBIOLOGY 47: 481 (1981). (10.1007/BF00443236) / ANTONIE VAN LEEUWENHOEK JOURNAL OF MICROBIOLOGY (1981)

Dates

Type	When
Created	18 years, 11 months ago (Oct. 5, 2006, 4:28 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 4:22 a.m.)
Indexed	2 months, 2 weeks ago (June 17, 2025, 11:29 a.m.)
Issued	39 years, 8 months ago (Jan. 3, 1986)
Published	39 years, 8 months ago (Jan. 3, 1986)
Published Print	39 years, 8 months ago (Jan. 3, 1986)

Funders 0

None

BibTeX

@article{Miller_1986, title={Osmotic Adaptation by Gram-Negative Bacteria: Possible Role for Periplasmic Oligosaccharides}, volume={231}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.3941890}, DOI={10.1126/science.3941890}, number={4733}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Miller, Karen J. and Kennedy, Eugene P. and Reinhold, Vernon N.}, year={1986}, month=jan, pages={48–51} }

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