Abstract
Anabaena variabilis ATCC 29413 is a heterotrophic, nitrogen-fixing cyanobacterium containing both a Mo-dependent nitrogenase encoded by the nif genes and V-dependent nitrogenase encoded by the vnf genes. The nifB, nifS, and nifU genes of A. variabilis were cloned, mapped, and partially sequenced. The fdxN gene was between nifB and nifS. Growth and acetylene reduction assays using wild-type and mutant strains indicated that the nifB product (NifB) was required for nitrogen fixation not only by the enzyme encoded by the nif genes but also by the enzyme encoded by the vnf genes. Neither NifS nor NifU was essential for nitrogen fixation in A. variabilis.
References
56
Referenced
51
-
Allen , M. B. , and D. I. Arnon . 1955 . Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm . Plant Physiol. (Bethesda) 30 : 366 - 372 .
(
10.1104/pp.30.4.366
) / Plant Physiol. (Bethesda) / Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm by Allen M. B. (1955) -
Allen , M. M. 1968 . Simple conditions for the growth of unicellular blue-green algae on plates . J. Phycol. 4 : 1 - 4 .
(
10.1111/j.1529-8817.1968.tb04667.x
) / J. Phycol. / Simple conditions for the growth of unicellular blue-green algae on plates by Allen M. M. (1968) -
Bancroft , I. , and C. P. Wolk . 1989 . Characterization of an insertion sequence (IS891) of novel structure from the cyanobacterium Anabaena sp. strain M-131 . J. Bacteriol. 171 : 5949 - 5954 .
(
10.1128/JB.171.11.5949-5954.1989
) / J. Bacteriol. / Characterization of an insertion sequence (IS891) of novel structure from the cyanobacterium Anabaena sp. strain M-131 by Bancroft I. (1989) -
Bauer , C. C. , L. Scappino , and Robert Haselkorn. 1994 . Growth of the cyanobacterium Anabaena on molecular nitrogen: NifJ is required when iron is limited . Proc. Natl. Acad. Sci. USA 90 : 8812 - 8816 .
(
10.1073/pnas.90.19.8812
) / Proc. Natl. Acad. Sci. USA / Growth of the cyanobacterium Anabaena on molecular nitrogen: NifJ is required when iron is limited by Bauer C. C. (1994) -
Beynon , J. , A. Ally , M. Cannon , F. Cannon , M. R. Jacobson , V. L. Cash , and D. Dean . 1987 . Comparative organization of nitrogen fixation-specific genes from Azotobacter vinelandii and Klebsiella pneumoniae: DNA sequence of the nifUSV genes . J. Bacteriol. 169 : 4024 - 4029 .
(
10.1128/JB.169.9.4024-4029.1987
) / J. Bacteriol. / Comparative organization of nitrogen fixation-specific genes from Azotobacter vinelandii and Klebsiella pneumoniae: DNA sequence of the nifUSV genes by Beynon J. (1987) - Bishop P. E. and R. Premakumar. 1992. Alternative nitrogen fixation systems p. 736-762. In G. Stacey R. H. Burris and H. J. Evans (ed.) Biological nitrogen fixation. Chapman & Hall Inc. New York.
-
Black , T. , Y. P. Cai , and C. P. Wolk . 1993 . Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol. Microbiol. 9 : 77 - 84 .
(
10.1111/j.1365-2958.1993.tb01670.x
) / Anabaena. Mol. Microbiol. / Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development by Black T. (1993) -
Böhme , H. , and R. Haselkorn . 1988 . Molecular cloning and nucleotide sequence analysis of the gene coding for heterocyst ferredoxin from the cyanobacterium Anabaena sp. strain PCC 7120 . Mol. Gen. Genet. 214 : 278 - 285 .
(
10.1007/BF00337722
) / Mol. Gen. Genet. / Molecular cloning and nucleotide sequence analysis of the gene coding for heterocyst ferredoxin from the cyanobacterium Anabaena sp. strain PCC 7120 by Böhme H. (1988) -
Brusca , J. S. , M. A. Hale , C. D. Carrasco , and J. W. Golden . 1989 . Excision of an 11-kilobase-pair DNA element from within the nifD gene in Anabaena variabilis heterocysts . J. Bacteriol. 171 : 4138 - 4145 .
(
10.1128/jb.171.8.4138-4145.1989
) / J. Bacteriol. / Excision of an 11-kilobase-pair DNA element from within the nifD gene in Anabaena variabilis heterocysts by Brusca J. S. (1989) -
Chisnell , J. R. , R. Premakumar , and P. E. Bishop . 1988 . Purification of a second alternative nitrogenase from a nifHDK deletion strain of Azotobacter vinelandii . J. Bacteriol. 170 : 27 - 33 .
(
10.1128/JB.170.1.27-33.1988
) / J. Bacteriol. / Purification of a second alternative nitrogenase from a nifHDK deletion strain of Azotobacter vinelandii by Chisnell J. R. (1988) -
Currier , T. C. , and C. P. Wolk . 1979 . Characteristics of Anabaena variabilis influencing plaque formation by cyanophage N-1 . J. Bacteriol. 139 : 88 - 92 .
(
10.1128/JB.139.1.88-92.1979
) / J. Bacteriol. / Characteristics of Anabaena variabilis influencing plaque formation by cyanophage N-1 by Currier T. C. (1979) -
Dean , D. R. , J. T. Bolin , and L. Zheng . 1993 . Nitrogenase metalloclusters: structures, organization, and synthesis . J. Bacteriol. 175 : 6737 - 6744 .
(
10.1128/JB.175.21.6737-6744.1993
) / J. Bacteriol. / Nitrogenase metalloclusters: structures, organization, and synthesis by Dean D. R. (1993) - Dean D. R. and M. R. Jacobson. 1992. Biochemical genetics of nitrogenase p. 763-834. In G. Stacey R. H. Burris and H. J. Evans (ed.) Biological nitrogen fixation. Chapman & Hall Inc. New York.
-
Dilworth , M. J. , R. R. Eady , and M. E. Eldridge . 1988 . The vanadium nitrogenase of Azotobacter chroococcum: reduction of acetylene and ethylene to ethane . Biochem. J. 249 : 745 - 751 .
(
10.1042/bj2490745
) / Biochem. J. / The vanadium nitrogenase of Azotobacter chroococcum: reduction of acetylene and ethylene to ethane by Dilworth M. J. (1988) -
Dilworth , M. J. , R. R. Eady , R. L. Robson , and R. W. Miller . 1987 . Ethane formation from acetylene as a potential test for vanadium nitrogenase in vivo . Nature (London) 27 : 167 - 168 .
(
10.1038/327167a0
) / Nature (London) / Ethane formation from acetylene as a potential test for vanadium nitrogenase in vivo by Dilworth M. J. (1987) -
Elhai , J. , and C. P. Wolk . 1988 . A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers . Gene 68 : 119 - 138 .
(
10.1016/0378-1119(88)90605-1
) / Gene / A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers by Elhai J. (1988) -
Feinberg , A. P. , and B. Vogelstein . 1983 . A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity . Anal. Biochem. 132 : 6 - 13 .
(
10.1016/0003-2697(83)90418-9
) / Anal. Biochem. / A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity by Feinberg A. P. (1983) -
Fleming , H. , and R. Haselkorn . 1973 . Differentiation in Noctoc muscorum: nitrogenase is synthesized in heterocysts . Proc. Natl. Acad. Sci. USA 70 : 2727 - 2731 .
(
10.1073/pnas.70.10.2727
) / Proc. Natl. Acad. Sci. USA / Differentiation in Noctoc muscorum: nitrogenase is synthesized in heterocysts by Fleming H. (1973) -
Golden , J. W. , M. E. Mulligan , and R. Haselkorn . 1987 . Different recombination site specificity of two developmentally regulated genome rearrangements . Nature (London) 327 : 526 - 529 .
(
10.1038/327526a0
) / Nature (London) / Different recombination site specificity of two developmentally regulated genome rearrangements by Golden J. W. (1987) -
Golden , J. W. , S. J. Robinson , and R. Haselkorn . 1985 . Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena . Nature (London) 314 : 419 - 423 .
(
10.1038/314419a0
) / Nature (London) / Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena by Golden J. W. (1985) -
Golden , J. W. , and D. R. Wiest . 1988 . Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene . Science 242 : 1421 - 1423 .
(
10.1126/science.3144039
) / Science / Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene by Golden J. W. (1988) -
Golden , S. S. , J. Brusslan , and R. Haselkorn . 1987 . Genetic engineering of the cyanobacterial chromosome . Methods Enzymol. 153 : 215 - 231 .
(
10.1016/0076-6879(87)53055-5
) / Methods Enzymol. / Genetic engineering of the cyanobacterial chromosome by Golden S. S. (1987) - Haselkorn R. and W. J. Buikema. 1992. Nitrogen fixation in cyanobacteria p. 166-190. In G. Stacey R. H. Burris and H. J. Evans (ed.) Biological nitrogen fixation. Chapman & Hall Inc. New York.
-
Herrero , A. , and C. P. Wolk . 1986 . Genetic mapping of the chromosome of the cyanobacterium, Anabaena variabilis. Proximity of the structural genes for nitrogenase and ribulosebisphosphate carboxylase . J. Biol. Chem. 261 : 7748 - 7754 .
(
10.1016/S0021-9258(19)57464-6
) / J. Biol. Chem. / Genetic mapping of the chromosome of the cyanobacterium, Anabaena variabilis. Proximity of the structural genes for nitrogenase and ribulosebisphosphate carboxylase by Herrero A. (1986) - Jackman D. M. and M. E. Mulligan. Unpublished data.
-
Jacobson , M. R. , V. L. Cash , M. C. Weiss , N. F. Laird , W. E. Newton , and D. R. Dean . 1989 . Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii . Mol. Gen. Genet. 219 : 49 - 57 .
(
10.1007/BF00261156
) / Mol. Gen. Genet. / Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii by Jacobson M. R. (1989) -
Joerger , R. D. , and P. E. Bishop . 1988 . Bacterial alternative nitrogen fixation systems . Crit. Rev. Microbiol. 16 : 1 - 14 .
(
10.3109/10408418809104465
) / Crit. Rev. Microbiol. / Bacterial alternative nitrogen fixation systems by Joerger R. D. (1988) -
Joerger , R. D. , and P. E. Bishop . 1988 . Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii . J. Bacteriol. 170 : 1475 - 1487 .
(
10.1128/JB.170.4.1475-1487.1988
) / J. Bacteriol. / Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii by Joerger R. D. (1988) -
Kennedy , C. , and D. Dean . 1992 . The nifU, nifS, and nifV gene products are required for activity of all three nitrogenases of Azotobacter vinelandii . Mol. Gen. Genet. 231 : 494 - 498 .
(
10.1007/BF00292722
) / Mol. Gen. Genet. / The nifU, nifS, and nifV gene products are required for activity of all three nitrogenases of Azotobacter vinelandii by Kennedy C. (1992) -
Lammers , P. J. , and R. Haselkorn . 1983 . Sequence of the nifD gene coding for thesubunit of dinitrogenase from the cyanobacterium Anabaena . Proc. Natl. Acad. Sci. USA 80 : 4723 - 4727 .
(
10.1073/pnas.80.15.4723
) / Proc. Natl. Acad. Sci. USA / Sequence of the nifD gene coding for thesubunit of dinitrogenase from the cyanobacterium Anabaena by Lammers P. J. (1983) -
MacKinney , G. 1941 . Absorption of light by chlorophyll solutions . J. Biol. Chem. 140 : 315 - 322 .
(
10.1016/S0021-9258(18)51320-X
) / J. Biol. Chem. / Absorption of light by chlorophyll solutions by MacKinney G. (1941) -
Masepohl , B. W. , S. Angermuller , S. Hennecke , P. Hubner , C. Morenovivian , and W. Klipp . 1993 . Nucleotide sequence and genetic analysis of the Rhodobacter capsulatus ORF6-nifUISVW gene region: possible role of NifW in homocitrate processing . Mol. Gen. Genet. 238 : 369 - 382 .
(
10.1007/BF00291996
) / Mol. Gen. Genet. / Nucleotide sequence and genetic analysis of the Rhodobacter capsulatus ORF6-nifUISVW gene region: possible role of NifW in homocitrate processing by Masepohl B. W. (1993) -
Mazur , B. , and C. F. Chui . 1982 . Sequence of the gene coding for the ~ subunit of dinitrogenase from the blue-green alga Anabaena . Proc. Natl. Acad. Sci. USA 79 : 6782 - 6786 .
(
10.1073/pnas.79.22.6782
) / Proc. Natl. Acad. Sci. USA / Sequence of the gene coding for the ~ subunit of dinitrogenase from the blue-green alga Anabaena by Mazur B. (1982) - Merrick , M. , M. Filser , R. Dixon , C. Elmerich , L. Sibold , and J. Houmard . 1980 . The use of translocatable genetic elements to construct a fine-structure map of the Klebsiella pneumoniae nitrogen fixation (nif) gene cluster . J. Gen. Microbiol. 117 : 509 - 520 . / J. Gen. Microbiol. / The use of translocatable genetic elements to construct a fine-structure map of the Klebsiella pneumoniae nitrogen fixation (nif) gene cluster by Merrick M. (1980)
-
Miller , A. - F. , and W. H. Orme-Johnson . 1992 . The dependence on iron availability of allocation of iron to nitrogenase components in Klebsiella pneumoniae and Escherichia coli . J. Biol. Chem. 267 : 9398 - 9408 .
(
10.1016/S0021-9258(19)50437-9
) / J. Biol. Chem. / The dependence on iron availability of allocation of iron to nitrogenase components in Klebsiella pneumoniae and Escherichia coli by Miller A. (1992) -
Mulligan , M. E. , W. J. Buikema , and R. Haselkorn . 1988 . Bacterial-type ferredoxin genes in the nitrogen fixation regions of the cyanobacterium Anabaena sp. strain PCC 7120 and Rhizobium meliloti . J. Bacteriol. 170 : 4406 - 4410 .
(
10.1128/JB.170.9.4406-4410.1988
) / J. Bacteriol. / Bacterial-type ferredoxin genes in the nitrogen fixation regions of the cyanobacterium Anabaena sp. strain PCC 7120 and Rhizobium meliloti by Mulligan M. E. (1988) -
Mulligan , M. E. , and R. Haselkorn . 1989 . Nitrogen fixation (nif) genes of the cyanobacterium Anabaena species strain PCC 7120: the nifB-fdxN-nifS-nifU operon . J. Biol. Chem. 264 : 19200 - 19207 .
(
10.1016/S0021-9258(19)47287-6
) / J. Biol. Chem. / Nitrogen fixation (nif) genes of the cyanobacterium Anabaena species strain PCC 7120: the nifB-fdxN-nifS-nifU operon by Mulligan M. E. (1989) -
Murry , M. A. , A. J. Horne , and J. R. Benemann . 1984 . Physiological studies of oxygen protection mechanisms in the heterocysts of Anabaena cylindrica . Appl. Environ. Microbiol. 47 : 449 - 454 .
(
10.1128/AEM.47.3.449-454.1984
) / Appl. Environ. Microbiol. / Physiological studies of oxygen protection mechanisms in the heterocysts of Anabaena cylindrica by Murry M. A. (1984) -
Murry , M. A. , and C. P. Wolk . 1989 . Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope . Arch. Microbiol. 151 : 469 - 474 .
(
10.1007/BF00454860
) / Arch. Microbiol. / Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope by Murry M. A. (1989) -
Peterson , R. B. , E. Dolan , H. E. Calvert , and B. Ke. 1981 . Energy transfer from phycobiliproteins to photosystem I in vegetative cells and heterocysts of Anabaena variabilis . Biochim. Biophys. Acta 634 : 237 - 248 .
(
10.1016/0005-2728(81)90142-0
) / Biochim. Biophys. Acta / Energy transfer from phycobiliproteins to photosystem I in vegetative cells and heterocysts of Anabaena variabilis by Peterson R. B. (1981) -
Peterson , R. B. , and C. P. Wolk . 1978 . High recovery of nitrogenase activity and of55Fe-labeled nitrogenase in heterocysts isolated from Anabaena variabilis . Proc. Natl. Acad. Sci. USA 75 : 6271 - 6275 .
(
10.1073/pnas.75.12.6271
) / Proc. Natl. Acad. Sci. USA / High recovery of nitrogenase activity and of55Fe-labeled nitrogenase in heterocysts isolated from Anabaena variabilis by Peterson R. B. (1978) -
Rice , D. , B. J. Mazur , and R. Haselkorn . 1982 . Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120 . J. Biol. Chem. 257 : 13157 - 13163 .
(
10.1016/S0021-9258(18)33636-6
) / J. Biol. Chem. / Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120 by Rice D. (1982) -
Roberts , G. P. , and W. J. Brill . 1980 . Gene-product relationships of the nif regulon of Klebsiella pneumoniae . J. Bacteriol. 144 : 210 - 216 .
(
10.1128/jb.144.1.210-216.1980
) / J. Bacteriol. / Gene-product relationships of the nif regulon of Klebsiella pneumoniae by Roberts G. P. (1980) -
Roberts , G. P. , T. MacNeil , D. MacNeil , and W. J. Brill . 1978 . Regulation and characterization of protein products coded by the nif (nitrogen fixation) genes of Klebsiella pneumoniae . J. Bacteriol. 136 : 267 - 279 .
(
10.1128/JB.136.1.267-279.1978
) / J. Bacteriol. / Regulation and characterization of protein products coded by the nif (nitrogen fixation) genes of Klebsiella pneumoniae by Roberts G. P. (1978) -
Rodríguez-Quiones , F. , R. Bosch , and J. Imperial . 1993 . Expression of the nifBfdxNnifOQ region of Azotobacter vinelandii and its role in nitrogenase activity . J. Bacteriol. 175 : 2926 - 2935 .
(
10.1128/JB.175.10.2926-2935.1993
) / J. Bacteriol. / Expression of the nifBfdxNnifOQ region of Azotobacter vinelandii and its role in nitrogenase activity by Rodríguez-Quiones F. (1993) - Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
-
Schneider , K. , A. Müller , K. -U. Johannes , E. Diemann , and J. Kottmann . 1991 . Selective removal of molybdenum traces from growth media of N2- fixing bacteria . Anal. Biochem. 193 : 292 - 298 .
(
10.1016/0003-2697(91)90024-N
) / Anal. Biochem. / Selective removal of molybdenum traces from growth media of N2- fixing bacteria by Schneider K. (1991) -
Schuddenkopf , K. M. , S. Hennecke , U. Liese , M. Kutsche , and W. Klipp . 1993 . Characterization of anf genes specific for the alternative nitrogenase and identification of nif genes required for both nitrogenases in Rhodobacter capsulatus . Mol. Microbiol. 8 : 673 - 684 .
(
10.1111/j.1365-2958.1993.tb01611.x
) / Mol. Microbiol. / Characterization of anf genes specific for the alternative nitrogenase and identification of nif genes required for both nitrogenases in Rhodobacter capsulatus by Schuddenkopf K. M. (1993) -
Shah , V. K. , J. R. Allen , N. J. Spangler , and P. W. Ludden . 1994 . In-vitro synthesis of the iron-molybdenum cofactor of nitrogenase: purification and characterization of NifB cofactor, the product of NifB protein . J. Biol. Chem. 269 : 1154 - 1158 .
(
10.1016/S0021-9258(17)42235-6
) / J. Biol. Chem. / In-vitro synthesis of the iron-molybdenum cofactor of nitrogenase: purification and characterization of NifB cofactor, the product of NifB protein by Shah V. K. (1994) - Shah V. K. T. R. Hoover J. Imperial T. D. Paustian G. P. Roberts and P. W. Ludden. 1988. Role of nif gene products and homocitrate in the biosynthesis of iron-molybdenum cofactor p. 115-120. In H. Bothe F. de Bruijn and W. Newton (ed.) Nitrogen fixation: a hundred years after. Gustav Fischer New York.
-
Sun , D. , and P. Setlow . 1993 . Cloning, nucleotide sequence, and regulation of the Bacillus subtilis nadB gene and a nifS-like gene, both of which are essential for NAD biosynthesis . J. Bacteriol. 175 : 1423 - 1432 .
(
10.1128/JB.175.5.1423-1432.1993
) / J. Bacteriol. / Cloning, nucleotide sequence, and regulation of the Bacillus subtilis nadB gene and a nifS-like gene, both of which are essential for NAD biosynthesis by Sun D. (1993) - Thiel T. Unpublished data.
-
Thiel , T. 1993 . Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis . J. Bacteriol. 175 : 6276 - 6286 .
(
10.1128/JB.175.19.6276-6286.1993
) / J. Bacteriol. / Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis by Thiel T. (1993) -
Thiel , T. , J. Bramble , and S. Rogers . 1989 . Optimum conditions for growth of cyanobacteria on solid media . FEMS Microbiol. Lett. 61 : 27 - 32 .
(
10.1111/j.1574-6968.1989.tb03546.x
) / FEMS Microbiol. Lett. / Optimum conditions for growth of cyanobacteria on solid media by Thiel T. (1989) -
Ugalde , R. A. , J. Imperial , V. H. Shah , and W. J. Brill . 1984 . Biosynthesis of iron-molybdenum cofactor in the absence of nitrogenase . J. Bacteriol. 159 : 888 - 893 .
(
10.1128/JB.159.3.888-893.1984
) / J. Bacteriol. / Biosynthesis of iron-molybdenum cofactor in the absence of nitrogenase by Ugalde R. A. (1984) -
Zheng , L. , R. H. White , V. L. Cash , R. F. Jack , and D. R. Dean . 1993 . Cysteine desulfurase activity indicates a role for nifS in metallocluster biosynthesis . Proc. Natl. Acad. Sci. USA 90 : 2754 - 2758 .
(
10.1073/pnas.90.7.2754
) / Proc. Natl. Acad. Sci. USA / Cysteine desulfurase activity indicates a role for nifS in metallocluster biosynthesis by Zheng L. (1993)
Dates
Type | When |
---|---|
Created | 8 years, 9 months ago (Nov. 9, 2016, 11:23 a.m.) |
Deposited | 4 years, 1 month ago (July 29, 2021, 1:55 p.m.) |
Indexed | 4 weeks, 2 days ago (Aug. 5, 2025, 8:11 a.m.) |
Issued | 30 years, 6 months ago (March 1, 1995) |
Published | 30 years, 6 months ago (March 1, 1995) |
Published Print | 30 years, 6 months ago (March 1, 1995) |
@article{Lyons_1995, title={Characterization of nifB, nifS, and nifU genes in the cyanobacterium Anabaena variabilis: NifB is required for the vanadium-dependent nitrogenase}, volume={177}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.177.6.1570-1575.1995}, DOI={10.1128/jb.177.6.1570-1575.1995}, number={6}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Lyons, E M and Thiel, T}, year={1995}, month=mar, pages={1570–1575} }