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Cellulose biosynthesis and function in bacteria
Open accessAbstract
The current model of cellulose biogenesis in plants, as well as bacteria, holds that the membranous cellulose synthase complex polymerizes glucose moieties from UDP-Glc into beta-1,4-glucan chains which give rise to rigid crystalline fibrils upon extrusion at the outer surface of the cell. The distinct arrangement and degree of association of the polymerizing enzyme units presumably govern extracellular chain assembly in addition to the pattern and width of cellulose fibril deposition. Most evident for Acetobacter xylinum, polymerization and assembly appear to be tightly coupled. To date, only bacteria have been effectively studied at the biochemical and genetic levels. In A. xylinum, the cellulose synthase, composed of at least two structurally similar but functionally distinct subunits, is subject to a multicomponent regulatory system. Regulation is based on the novel nucleotide cyclic diguanylic acid, a positive allosteric effector, and the regulatory enzymes maintaining its intracellular turnover: diguanylate cyclase and Ca2(+)-sensitive bis-(3',5')-cyclic diguanylic acid (c-di-GMP) phosphodiesterase. Four genes have been isolated from A. xylinum which constitute the operon for cellulose synthesis. The second gene encodes the catalytic subunit of cellulose synthase; the functions of the other three gene products are still unknown. Exclusively an extracellular product, bacterial cellulose appears to fulfill diverse biological roles within the natural habitat, conferring mechanical, chemical, and physiological protection in A. xylinum and Sarcina ventriculi or facilitating cell adhesion during symbiotic or infectious interactions in Rhizobium and Agrobacterium species. A. xylinum is proving to be most amenable for industrial purposes, allowing the unique features of bacterial cellulose to be exploited for novel product applications.
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“Bacterial cellulose (BC), produced by acetic acid bacteria Gluconobacter xylinum, is obtainable in a pure form which requires no intensive processing to remove undesirable impurities and contaminants such as lignin, pectin and hemicellulose.75,76”
From Sustainable hybrid photocatalysts: titania immobilized on carbon materials derived from renewable and biodegradable resources (2016) · cites this paper as [76]
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“In such an analysis, however, the effect of substitutions on the overall conformation of the molecule is not taken into account; cyclic dinucleotides can adopt a variety of asymmetrical conformations in solution (24) and in the crystalline state (53); this necessarily limits many conclusions regarding the structure-fu…”
BackgroundRegulation of hexose phosphate metabolism in Acetobacter xylinum.
Weinhouse, H., & Benziman, M. (1974) · Biochemical Journal · doi:10.1042/bj1380537 · Cited by 28
Self-citationDeveloping a hypothesis: Native cellulose elementary fibrils are formed with metastable structure
Stöckmann, V. E. (1972) · doi:10.1002/bip.1972.360110119 · Cited by 28
Characterization and Properties of the Pyruvate Phosphorylation System of Acetobacter xylinum
Benziman, M., & Palgi, A. (1970) · Journal of Bacteriology · doi:10.1128/jb.104.1.211-218.1970 · Cited by 28 · cited 1×
“Within the cell, PP, is rapidly cleaved to yield Pi (18).”
BackgroundSelf-citationFactors afecting the activity of pyruvate kinase of Acetobacter xylinum.
Benziman, M. (1969) · Biochemical Journal · doi:10.1042/bj1120631 · Cited by 28 · cited 1×
“mutase (60); 9, glucose-6-P1-dehydrogenase (NAD); 9a, glucose-6-Pi-dehydrogenase (NADP) (17); 10, 6-phosphogluconate dehydrogenase (NAD); 10a, 6-phosphogluconate dehydrogenase (NADP); 11, phosphoglucoisomerase; 12, phosphoribulose epimerase; 13, phosphoribulose isomerase; 14, transketolase; 15, transaldolase (60); 16,…”
Self-citationFactors Affecting Hexose Phosphorylation in Acetobacter xylinum
Benziman, M., & Rivetz, B. (1972) · Journal of Bacteriology · doi:10.1128/jb.111.2.325-333.1972 · Cited by 28 · cited 4×
“1, Cellulose synthase (2, 115); 2, glucose oxidase (60); 3, glucose permease; 4, gluconate permease (19); 5, UDPG-pyrophosphorylase (UTP) (143); 6, glucokinase (ATP) (19); 7, gluconokinase (ATP); 8, phosphogluco-”
BackgroundInfluentialSelf-citationCarbohydrate Metabolism in Agrobacterium tumefaciens
Arthur, L., Bulla, L., Julian, G. S., et al. (1973) · Journal of Bacteriology · doi:10.1128/jb.116.1.304-313.1973 · Cited by 27
Purification and Regulatory Properties of the Oxaloacetate Decarboxylase of Acetobacter xylinum
Benziman, M., Russo, A., Hochman, S., et al. (1978) · Journal of Bacteriology · doi:10.1128/jb.134.1.1-9.1978 · Cited by 26 · cited 2×
“mutase (60); 9, glucose-6-P1-dehydrogenase (NAD); 9a, glucose-6-Pi-dehydrogenase (NADP) (17); 10, 6-phosphogluconate dehydrogenase (NAD); 10a, 6-phosphogluconate dehydrogenase (NADP); 11, phosphoglucoisomerase; 12, phosphoribulose epimerase; 13, phosphoribulose isomerase; 14, transketolase; 15, transaldolase (60); 16,…”
BackgroundSelf-citationTunnel structures in Acetobacter xylinum
Thompson, N. S., Carlson, J. A., Kaustinen, H., et al. (1988) · doi:10.1016/0141-8130(88)90021-9 · Cited by 24
Koreeda, A., Harada, T., Ogawa, K., et al. (1974) · doi:10.1016/s0008-6215(00)82823-2 · Cited by 24 · cited 1×
“is synthesized simultaneously with other exopolysaccharides, including curdlan, a P-1,3-glucan which appears to contain some degree of organized tertiary structure and yields insoluble gels (86).”
BackgroundWhitfield, C., Adams, D. A., & Troy, F. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90812-4 · Cited by 21
Cooper, D., & Manley, R. (1975) · Biochimica et Biophysica Acta · doi:10.1016/0304-4165(75)90192-0 · Cited by 21 · cited 1×
“This is in contradiction to previously proposed models in which intramembranous particles that were revealed by freeze-etching of the cell envelope were taken to indicate that cellulose synthase is located in the outer membrane (28, 38).”
ResultFLAVINE ADENINE DINUCLEOTIDE-LINKED MALIC DEHYDROGENASE FROM ACETOBACTER XYLINUM
Benziman, M., & Galanter, Y. (1964) · Journal of Bacteriology · doi:10.1128/jb.88.4.1010-1018.1964 · Cited by 20
Self-citationHotchkiss, A. (1989) · doi:10.1021/bk-1989-0399.ch017 · Cited by 19 · cited 1×
“The biological occurrence of terminal complexes and rosettes has been classified according to phylogenetic history, wherein the distinction is made between fixed and mobile bigenetic apparatus (27, 77, 89).”
BackgroundAmemura, A. (1984) · doi:10.1271/bbb1961.48.1809 · Cited by 19 · cited 1×
“coli, in which the native products, known as membrane-derived oligosaccharides (MDOs), typically occur as ,8-1,6-branched derivatives in linkage to phosphoglyceride and/or succinate, as well as in membranous preparations from Agrobacterium radiobacter and Rhizobium phaseoli, in which the predominant in vivo species is…”
BackgroundDoes β-Glucan Synthesis Need a Primer?
Maclachlan, G. (1982) · doi:10.1007/978-1-4684-1116-4_16 · Cited by 19
Activities of citrate synthase and other enzymes of Acetobacter xylinum in situ and in vitro.
Swissa, M., Weinhouse, H., & Benziman, M. (1976) · Biochemical Journal · doi:10.1042/bj1530499 · Cited by 18
Self-citationRegulation of gluconeogenesis in Acetobacter xylinum.
Weinhouse, H., & Benziman, M. (1972) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1972.tb01886.x · Cited by 18
Self-citationRole of Phosphoenolpyruvate Carboxylation in Acetobacter xylinum
Benziman, M. (1969) · Journal of Bacteriology · doi:10.1128/jb.98.3.1005-1010.1969 · Cited by 18 · cited 1×
“mutase (60); 9, glucose-6-P1-dehydrogenase (NAD); 9a, glucose-6-Pi-dehydrogenase (NADP) (17); 10, 6-phosphogluconate dehydrogenase (NAD); 10a, 6-phosphogluconate dehydrogenase (NADP); 11, phosphoglucoisomerase; 12, phosphoribulose epimerase; 13, phosphoribulose isomerase; 14, transketolase; 15, transaldolase (60); 16,…”
Self-citationLipid-bound saccharides containing glucose and galactose in Agrobacterium tumefaciens
Staneloni, R., Tolmasky, M., & Leloir, L. (1984) · doi:10.1099/00221287-130-4-869 · Cited by 16 · cited 1×
“corresponding polyprenol diphosphate saccharide, which grows from the addition of galactose followed by glucosylation in a sequence of,B-1,4, ,B-1,6, and 1-1,3 bonding, as determined in vitro by using radiolabeled UDP-Glc or UDPGal as a substrate (131).”
MethodSwissa, M., & Benziman, M. (1976) · Biochemical Journal · doi:10.1042/bj1530173 · Cited by 15
Self-citationCellulose and β-Glucan Synthesis in Saprolegnia
Fěvre, M., Girard, V., & Nodet, P. (1990) · doi:10.1007/978-3-642-74215-6_7 · Cited by 15
β‐1,2‐Glucosyl transfer by membrane preparations from acetobacter xylinum
Sandermann, H., & Dekker, R. F. H. (1979) · FEBS Letters · doi:10.1016/0014-5793(79)80504-9 · Cited by 14 · cited 2×
“xylinum strains have also been observed to utilize UDPGlc in forming a high-molecular-weight P-1,2-homoglucan (117); however, such a material has been detected in only”
BackgroundEffect of culture conditions of acetic acid bacteria on cellulose biosynthesis
Kamide, K., Matsuda, Y., Iijima, H., et al. (1990) · doi:10.1002/pi.4980220212 · Cited by 14 · cited 1×
“occurs at a rate that is linear with respect to the cell concentration (73, 81) and, as mentioned above, is constitutive with respect to the carbon source supplied for cell FIG.”
BackgroundThe extracellular proteins of Acetobacter xylinum and their relationship to cellulose synthesis.
Webb, T., & Colvin, J. (1967) · Canadian Journal of Biochemistry · doi:10.1139/o67-055 · Cited by 12
Intermediates of Cellulose Synthesis in Acetobacter
Aloni, Y., & Benziman, M. (1982) · doi:10.1007/978-1-4684-1116-4_17 · Cited by 12
Self-citationHisamatsu, M., Abe, J., Amemura, A., et al. (1980) · doi:10.1271/bbb1961.44.461 · Cited by 10 · cited 1×
“composed from an octasaccharide repeating unit containing glucose, galactose, and pyruvate in the ratio 7:1:1 (22, 74, 75, 158).”
BackgroundRuben, G., Bokelman, G. H., Krakow, W., et al. (1989) · doi:10.1021/bk-1989-0399.ch020 · Cited by 7
Comparisons between Synthetic and Natural Microfiber Systems
Sawyer, L., & George, W. (1982) · doi:10.1007/978-1-4684-1116-4_21 · Cited by 7 · cited 1×
“If individual ,-1,4glucan chains were synthesized in a disorganized, random fashion, the result would probably be a tangled mass in which any recognizable fibril structures contain chains associated in opposing directions or bent back upon themselves (119, 132).”
BackgroundStudies on Cellulose Metabolism (1970–1990)
Maclachlan, G. (1983) · doi:10.1007/978-94-009-6854-7_7 · Cited by 3
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“An extensive study of this process by Benziman and colleagues showed that it is regulated by cyclic diguanylate (c-diGMP, bis(3P,5P)-cyclic diguanylic acid), a novel e¡ector molecule that consists of two cGMP moieties bound head-to-tail [31].”
Background
Metadata
- Authors
- Ross, P., Mayer, R., & Benziman, M.
- Affiliations
- Hebrew University of Jerusalem (IL)
- Venue
- Microbiological Reviews
- Publisher
- American Society for Microbiology
- Published
- 1991-03
- Volume
- 55
- Issue
- 1
- Pages
- 35-58
- ISSN
- 0146-0749 (ISSN-L)
- PMC
- PMC372800
- OpenAlex
- W1911657064
- Cited by
- 1,231
- References
- 145
- Citations by year
- 2026: 18 · 2025: 43 · 2024: 45 · 2023: 64 · 2022: 67 · 2021: 74 · 2020: 56 · 2019: 59 · 2018: 60 · 2017: 56 · 2016: 48 · 2015: 70 · 2014: 67 · 2013: 53 · 2012: 47
- FWCI
- 8.86
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Locations
- Microbiological Reviews (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Materials Science › Biomaterials › Advanced Cellulose Research Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Polysaccharides and Plant Cell Walls
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- bacterial cellulose, cellulose biosynthesis, cellulose synthase, Acetobacter xylinum, c-di-GMP, diguanylate cyclase, c-di-GMP phosphodiesterase, allosteric regulation, Sarcina ventriculi, Rhizobium, Agrobacterium, cell adhesion
- MeSH terms
- Bacteria, Cellulose
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