DOI: 10.1128/jb.178.11.3293-3307.1996. Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family

Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family

10.1128/jb.178.11.3293-3307.1996

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

DNA sequencing and Southern blot analyses of a Borrelia burgdorferi DNA fragment encoding a signal sequence led to the discovery of a genetic locus, designated 2.9, which appears to be present in at least seven copies in virulent B. burgdorferi 297. DNA sequence analysis of these regions revealed that each 2.9 locus contained an operon of four genes (ABCD) and open reading frames designated rep+ (positive strand) and rep- (negative strand) which encoded multiple repeat motifs. Downstream of the rep+ gene(s) in six of the completely cloned and sequenced 2.9 loci also were lipoprotein (LP) genes possessing highly similar signal sequences but encoding variable mature polypeptides. The lipoproteins could he separated into two classes on the basis of hydrophilicity profiles, sequence similarities, and reactivity with specific antibodies. The 2.9 loci were localized to two (20- and 30-kb) supercoiled plasmids in B. burgdorferi 297. Northern (RNA) blot analysis established that the 2.9 ABCD operon was only minimally expressed, whereas the rep- gene(s) and at least three of the seven LP genes were expressed by B. burgdorferi in vitro. A single putative promoter element was identified by RNA primer extension analysis upstream of the ABCD operon, whereas a number of potential promoter regions existed upstream of the LP genes. The combined data indicate that the ABCD operon, rep+ and rep- genes, and LP genes are separately transcribed during in vitro growth. The 2.9 loci possess a repetitiveness, diversity, and complexity not previously described for B. burgdorferi; differential expression of these genes may facilitate the spirochete's ability to survive in diverse host environments.

Bibliography

Porcella, S. F., Popova, T. G., Akins, D. R., Li, M., Radolf, J. D., & Norgard, M. V. (1996). Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family. Journal of Bacteriology, 178(11), 3293â3307.

Authors 6

S F Porcella (first)
T G Popova (additional)
D R Akins (additional)
M Li (additional)
J D Radolf (additional)
M V Norgard (additional)

References 54 Referenced 73

Akins D. R. S. F. Porcella M. V. Norgard and J. D. Radolf. 1996. Unpublished observations.
Akins , D. R. , S. F. Porcella , T. G. Popova , D. Shevchenko , S. I. Baker , M. Li , M. V. Norgard , and J. D. Radolf . 1995 . Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homolog . Mol. Microbiol. 18 : 507 - 520 . (10.1111/j.1365-2958.1995.mmi_18030507.x) / Mol. Microbiol. / Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homolog by Akins D. R. (1995)
Aron , L. , M. Alekshun , L. Perlee , I. Schwartz , H. P. Godfrey , and F. C. Cabello . 1994 . Cloning and DNA sequence analysis of bmpC, a gene encoding a potential membrane lipoprotein of Borrelia burgdorferi . FEMS Microbiol. Lett. 123 : 75 - 82 . (10.1111/j.1574-6968.1994.tb07204.x) / FEMS Microbiol. Lett. / Cloning and DNA sequence analysis of bmpC, a gene encoding a potential membrane lipoprotein of Borrelia burgdorferi by Aron L. (1994)
Barbour , A. G. 1984 . Isolation and cultivation of Lyme disease spirochetes . Yale J. Biol. Med. 57 : 521 - 525 . / Yale J. Biol. Med. / Isolation and cultivation of Lyme disease spirochetes by Barbour A. G. (1984)
Barbour , A. G. 1988 . Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent . J. Clin. Microbiol. 26 : 475 - 478 . (10.1128/jcm.26.3.475-478.1988) / J. Clin. Microbiol. / Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent by Barbour A. G. (1988)
Barbour , A. G. 1990 . Antigenic variation of a relapsing fever Borrelia species. Annu . Rev. Microbiol. 44 : 155 - 171 . (10.1146/annurev.mi.44.100190.001103) / Rev. Microbiol. / Antigenic variation of a relapsing fever Borrelia species. Annu by Barbour A. G. (1990)
Bergstrom , S. , V. G. Bundoc , and A. G. Barbour . 1989 . Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochaete Borrelia burgdorferi . Mol. Microbiol. 3 : 479 - 486 . (10.1111/j.1365-2958.1989.tb00194.x) / Mol. Microbiol. / Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochaete Borrelia burgdorferi by Bergstrom S. (1989)
Brandt , M. E. , B. S. Riley , J. D. Radolf , and M. V. Norgard . 1990 . Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins . Infect. Immun. 58 : 983 - 991 . (10.1128/iai.58.4.983-991.1990) / Infect. Immun. / Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins by Brandt M. E. (1990)
Bundoc , V. G. , and A. G. Barbour . 1989 . Clonal polymorphisms of outer membrane protein OspB of Borrelia burgdorferi . Infect. Immun. 57 : 2733 - 2741 . (10.1128/IAI.57.9.2733-2741.1989) / Infect. Immun. / Clonal polymorphisms of outer membrane protein OspB of Borrelia burgdorferi by Bundoc V. G. (1989)
Centers for Disease Control. 1993 . Lyme disease-United States, 1991-1992 . Morbid. Mortal. Weekly Rep. 42 : 345 - 348 . / Morbid. Mortal. Weekly Rep. / Lyme disease-United States, 1991-1992 by Centers for Disease Control. (1993)
Champion , C. I. , D. R. Blanco , J. T. Skare , D. A. Haake , M. Giladi , D. Foley , J. N. Miller , and M. A. Lovett . 1994 . A 9.0-kilobase-pair circular plasmid of Borrelia burgdorferi encodes an exported protein: evidence for expression only during infection . Infect. Immun. 62 : 2653 - 2661 . (10.1128/IAI.62.7.2653-2661.1994) / Infect. Immun. / A 9.0-kilobase-pair circular plasmid of Borrelia burgdorferi encodes an exported protein: evidence for expression only during infection by Champion C. I. (1994)
Devereux , J. , P. Haeberli , and O. Smithies . 1984 . A comprehensive set of sequence analysis programs for the VAX . Nucleic Acids Res. 12 : 387 - 395 . (10.1093/nar/12.1Part1.387) / Nucleic Acids Res. / A comprehensive set of sequence analysis programs for the VAX by Devereux J. (1984)
Dunn , J. J. , S. R. Buchstein , L. -L. Butler , S. Fisenne , D. S. Polin , B. N. Lade , and B. J. Luft . 1994 . Complete nucleotide sequence of a circular plasmid from the Lyme disease spirochete, Borrelia burgdorferi . J. Bacteriol. 176 : 2706 - 2717 . (10.1128/JB.176.9.2706-2717.1994) / J. Bacteriol. / Complete nucleotide sequence of a circular plasmid from the Lyme disease spirochete, Borrelia burgdorferi by Dunn J. J. (1994)
Engstrom , S. E. , E. Shoop , and R. C. Johnson . 1995 . Immunoblot interpretation criteria for serodiagnosis of early Lyme disease . J. Clin. Microbiol. 33 : 419 - 427 . (10.1128/JCM.33.2.419-427.1995) / J. Clin. Microbiol. / Immunoblot interpretation criteria for serodiagnosis of early Lyme disease by Engstrom S. E. (1995)
Ferdows , M. S. , and A. G. Barbour . 1989 . Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent . Proc. Natl. Acad. Sci. USA 86 : 5969 - 5973 . (10.1073/pnas.86.15.5969) / Proc. Natl. Acad. Sci. USA / Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent by Ferdows M. S. (1989)
Fuchs , R. , S. Jauris , F. Lottspeich , V. Preac-Mursic , B. Wilske , and E. Soutschek . 1992 . Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22kDa protein (pC) in Escherichia coli . Mol. Microbiol. 6 : 503 - 509 . (10.1111/j.1365-2958.1992.tb01495.x) / Mol. Microbiol. / Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22kDa protein (pC) in Escherichia coli by Fuchs R. (1992)
Garcia-Monco , J. C. , and J. L. Benach . 1995 . Lyme neuroborreliosis . Ann. Neurol. 37 : 691 - 702 . (10.1002/ana.410370602) / Ann. Neurol. / Lyme neuroborreliosis by Garcia-Monco J. C. (1995)
Gassmann , G. S. , M. Kramer , U. B. Gobel , and R. Wallich . 1989 . Nucleotide sequence of a gene encoding the Borrelia burgdorferi flagellin . Nucleic Acids Res. 17 : 3590 . (10.1093/nar/17.9.3590) / Nucleic Acids Res. / Nucleotide sequence of a gene encoding the Borrelia burgdorferi flagellin by Gassmann G. S. (1989)
Hechemy , K. E. , W. A. Samsonoff , H. L. Harris , and M. McKee . 1992 . Adherence and entry of Borrelia burgdorferi in Vero cells . J. Med. Microbiol. 36 : 229 - 238 . (10.1099/00222615-36-4-229) / J. Med. Microbiol. / Adherence and entry of Borrelia burgdorferi in Vero cells by Hechemy K. E. (1992)
Hoffman , C. S. , and A. Wright . 1985 . Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion . Proc. Natl. Acad. Sci. USA 82 : 5107 - 5111 . (10.1073/pnas.82.15.5107) / Proc. Natl. Acad. Sci. USA / Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion by Hoffman C. S. (1985)
Jonsson , M. , and S. Bergstrom . 1995 . Transcriptional and translational regulation of the expression of the major outer surface proteins in Lyme disease Borrelia strains . Microbiology 141 : 1321 - 1329 . (10.1099/13500872-141-6-1321) / Microbiology / Transcriptional and translational regulation of the expression of the major outer surface proteins in Lyme disease Borrelia strains by Jonsson M. (1995)
Kenney , T. J. , K. York , P. Youngman , and C. P. Moran , Jr. 1989 . Genetic evidence that RNA polymerase associated with sigma A factor uses a sporulation-specific promoter in Bacillus subtilis . Proc. Natl. Acad. Sci. USA 86 : 9109 - 9113 . (10.1073/pnas.86.23.9109) / Proc. Natl. Acad. Sci. USA / Genetic evidence that RNA polymerase associated with sigma A factor uses a sporulation-specific promoter in Bacillus subtilis by Kenney T. J. (1989)
Kurtti , T. J. , U. G. Munderloh , D. E. Krueger , R. C. Johnson , and T. G. Schwan . 1993 . Adhesion to and invasion of cultured tick (Acarina: Ixodidae) cells by Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) and maintenance of infectivity . J. Med. Entomol. 30 : 586 - 596 . (10.1093/jmedent/30.3.586) / J. Med. Entomol. / Adhesion to and invasion of cultured tick (Acarina: Ixodidae) cells by Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) and maintenance of infectivity by Kurtti T. J. (1993)
Lam , T. T. , T. P. K. Nguyen , R. R. Montgomery , F. S. Kantor , E. Fikrig , and R. A. Flavell . 1994 . Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease . Infect. Immun. 62 : 290 - 298 . (10.1128/IAI.62.1.290-298.1994) / Infect. Immun. / Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease by Lam T. T. (1994)
Lane , R. S. , J. Piesman , and W. Burgdorfer . 1991 . Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu. Rev. Entomol. 36 : 587 - 609 . (10.1146/annurev.en.36.010191.003103) / Europe. Annu. Rev. Entomol. / Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and by Lane R. S. (1991)
Liveris , D. , A. Gazumyan , and I. Schwartz . 1995 . Molecular typing of Borrelia burgdorferi sensu lato by PCR-restriction fragment length polymorphism analysis . J. Clin. Microbiol. 33 : 589 - 595 . (10.1128/JCM.33.3.589-595.1995) / J. Clin. Microbiol. / Molecular typing of Borrelia burgdorferi sensu lato by PCR-restriction fragment length polymorphism analysis by Liveris D. (1995)
Logigian , E. L. , R. F. Kaplan , and A. C. Steere . 1990 . Chronic neurologic manifestations of Lyme disease . N. Engl. J. Med. 323 : 1438 - 1444 . (10.1056/NEJM199011223232102) / N. Engl. J. Med. / Chronic neurologic manifestations of Lyme disease by Logigian E. L. (1990)
Margolis , N. , D. Hogan , K. Tilly , and P. A. Rosa . 1994 . Plasmid location of Borrelia purine biosynthesis gene homologs . J. Bacteriol. 176 : 6427 - 6432 . (10.1128/JB.176.21.6427-6432.1994) / J. Bacteriol. / Plasmid location of Borrelia purine biosynthesis gene homologs by Margolis N. (1994)
Moody , K. D. , S. W. Barthold , and G. A. Terwilliger . 1990 . Lyme borreliosis in laboratory animals: effect of host species and in vitro passage of Borrelia burgdorferi . Am. J. Trop. Med. Hyg. 43 : 87 - 92 . (10.4269/ajtmh.1990.43.87) / Am. J. Trop. Med. Hyg. / Lyme borreliosis in laboratory animals: effect of host species and in vitro passage of Borrelia burgdorferi by Moody K. D. (1990)
Mulligan , M. E. , D. K. Hawley , R. Entriken , and W. R. McClure . 1984 . Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity . Nucleic Acids Res. 12 : 789 - 800 . (10.1093/nar/12.1Part2.789) / Nucleic Acids Res. / Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity by Mulligan M. E. (1984)
Munderloh , U. G. , Y. -J. Park , J. M. Dioh , A. M. Fallon , and T. J. Kurtti . 1993 . Plasmid modifications in a tick-borne pathogen, Borrelia burgdorferi, cocultured with tick cells . Insect Mol. Biol. 1 : 195 - 203 . (10.1111/j.1365-2583.1993.tb00092.x) / Insect Mol. Biol. / Plasmid modifications in a tick-borne pathogen, Borrelia burgdorferi, cocultured with tick cells by Munderloh U. G. (1993)
Norris , S. J. , C. J. Carter , J. K. Howell , and A. G. Barbour . 1992 . Lowpassage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein . Infect. Immun. 60 : 4662 - 4672 . (10.1128/IAI.60.11.4662-4672.1992) / Infect. Immun. / Lowpassage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein by Norris S. J. (1992)
Ojaimi , C. , B. E. Davidson , I. Saint Girons , and I. G. Old . 1994 . Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii . Microbiology 140 : 2931 - 2940 . (10.1099/13500872-140-11-2931) / Microbiology / Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii by Ojaimi C. (1994)
Philipp M. T. 1996. Personal communication.
Pugsley , A. P. 1993 . The complete general secretory pathway in gram-negative bacteria . Microbiol. Rev. 57 : 50 - 108 . (10.1128/mr.57.1.50-108.1993) / Microbiol. Rev. / The complete general secretory pathway in gram-negative bacteria by Pugsley A. P. (1993)
Pugsley , A. P. , M. G. Kornacker , and I. Poquet . 1991 . The general proteinexport pathway is directly required for extracellular pullulanase secretion in Escherichia coli K12 . Mol. Microbiol. 5 : 343 - 352 . (10.1111/j.1365-2958.1991.tb02115.x) / Mol. Microbiol. / The general proteinexport pathway is directly required for extracellular pullulanase secretion in Escherichia coli K12 by Pugsley A. P. (1991)
Ray , C. , M. Igo , W. Shafer , R. Losick , and C. P. Moran , Jr. 1988 . Suppression of ctc promoter mutations in Bacillus subtilis . J. Bacteriol. 170 : 900 - 907 . (10.1128/jb.170.2.900-907.1988) / J. Bacteriol. / Suppression of ctc promoter mutations in Bacillus subtilis by Ray C. (1988)
Reindl , M. , B. Redl , and G. Stöffler . 1993 . Isolation and analysis of a linear plasmid-located gene of Borrelia burgdorferi B29 encoding a 27kDa surface lipoprotein (P27) and its overexpression in Escherichia coli . Mol. Microbiol. 8 : 1115 - 1124 . (10.1111/j.1365-2958.1993.tb01656.x) / Mol. Microbiol. / Isolation and analysis of a linear plasmid-located gene of Borrelia burgdorferi B29 encoding a 27kDa surface lipoprotein (P27) and its overexpression in Escherichia coli by Reindl M. (1993)
Sadziene , A. , B. Wilske , M. S. Ferdows , and A. G. Barbour . 1993 . The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid . Infect. Immun. 61 : 2192 - 2195 . (10.1128/IAI.61.5.2192-2195.1993) / Infect. Immun. / The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid by Sadziene A. (1993)
Saint Girons , I. , I. G. Old , and B. E. Davidson . 1994 . Molecular biology of the Borrelia, bacteria with linear replicons . Microbiology 140 : 1803 - 1816 . (10.1099/13500872-140-8-1803) / Microbiology / Molecular biology of the Borrelia, bacteria with linear replicons by Saint Girons I. (1994)
Schwan , T. G. , W. Burgdorfer , and C. F. Garon . 1988 . Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation . Infect. Immun. 56 : 1831 - 1836 . (10.1128/IAI.56.8.1831-1836.1988) / Infect. Immun. / Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation by Schwan T. G. (1988)
Schwan , T. G. , J. Piesman , W. T. Golde , M. C. Dolan , and P. A. Rosa . 1995 . Induction of an outer surface protein on Borrelia burgdorferi during tick feeding . Proc. Natl. Acad. Sci. USA 92 : 2909 - 2913 . (10.1073/pnas.92.7.2909) / Proc. Natl. Acad. Sci. USA / Induction of an outer surface protein on Borrelia burgdorferi during tick feeding by Schwan T. G. (1995)
Shoberg , R. J. , and D. D. Thomas . 1993 . Specific adherence of Borrelia burgdorferi extracellular vesicles to human endothelial cells in culture . Infect. Immun. 61 : 3892 - 3900 . (10.1128/IAI.61.9.3892-3900.1993) / Infect. Immun. / Specific adherence of Borrelia burgdorferi extracellular vesicles to human endothelial cells in culture by Shoberg R. J. (1993)
Simpson , W. J. , W. Cieplak , M. E. Schrumpf , A. G. Barbour , and T. G. Schwan . 1994 . Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen . FEMS Microbiol. Lett. 119 : 381 - 387 . (10.1111/j.1574-6968.1994.tb06917.x) / FEMS Microbiol. Lett. / Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen by Simpson W. J. (1994)
Simpson , W. J. , C. F. Garon , and T. G. Schwan . 1990 . Borrelia burgdorferi contains repeated DNA sequences that are species specific and plasmid associated . Infect. Immun. 58 : 847 - 853 . (10.1128/iai.58.4.847-853.1990) / Infect. Immun. / Borrelia burgdorferi contains repeated DNA sequences that are species specific and plasmid associated by Simpson W. J. (1990)
Sinsky , R. J. , and J. Piesman . 1989 . Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents . J. Clin. Microbiol. 27 : 1723 - 1727 . (10.1128/JCM.27.8.1723-1727.1989) / J. Clin. Microbiol. / Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents by Sinsky R. J. (1989)
Steere , A. C. 1989 . Lyme disease . N. Engl. J. Med. 321 : 586 - 597 . (10.1056/NEJM198908313210906) / N. Engl. J. Med. / Lyme disease by Steere A. C. (1989)
Stevenson B. K. Tilly and P. A. Rosa. J. Bacteriol. in press.
Suk , K. , S. Das , W. Sun , B. Jwang , S. W. Barthold , R. A. Flavell , and E. Fikrig . 1995 . Borrelia burgdorferi genes selectively expressed in the infected host . Proc. Natl. Acad. Sci. USA 92 : 4269 - 4273 . (10.1073/pnas.92.10.4269) / Proc. Natl. Acad. Sci. USA / Borrelia burgdorferi genes selectively expressed in the infected host by Suk K. (1995)
Swancutt , M. A. , J. D. Radolf , and M. V. Norgard . 1990 . The 34-kilodalton membrane immunogen of Treponema pallidum is a lipoprotein . Infect. Immun. 58 : 384 - 392 . (10.1128/IAI.58.2.384-392.1990) / Infect. Immun. / The 34-kilodalton membrane immunogen of Treponema pallidum is a lipoprotein by Swancutt M. A. (1990)
Swancutt , M. A. , B. S. Riley , J. D. Radolf , and M. V. Norgard . 1989 . Molecular characterization of the pathogen-specific 34-kilodalton membrane immunogen of Treponema pallidum . Infect. Immun. 57 : 3314 - 3323 . (10.1128/IAI.57.11.3314-3323.1989) / Infect. Immun. / Molecular characterization of the pathogen-specific 34-kilodalton membrane immunogen of Treponema pallidum by Swancutt M. A. (1989)
Wallich , R. , C. Brenner , M. D. Kramer , and M. M. Simon . 1995 . Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo . Infect. Immun. 63 : 3327 - 3335 . (10.1128/IAI.63.9.3327-3335.1995) / Infect. Immun. / Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo by Wallich R. (1995)
Zuckert W. R. E. Filipuzzi-Jenny M. Stalhammar-Carlemalm J. Melster-Turner and J. Meyer. 1994. Repeated DNA sequences on circular and linear plasmids of Borrelia burgdorferi sensu lato. p. 253-260. In J. S. Axford and D. H. E. Rees (ed.) Lyme borreliosis. Plenum Press New York. (10.1007/978-1-4615-2415-1_36)
Zuckert , W. R. , and J. Meyer . 1996 . Circular and linear plasmids of Lyme disease spirochetes share extensive homology: characterization of a repeated DNA element . J. Bacteriol. 178 : 2287 - 2298 . (10.1128/jb.178.8.2287-2298.1996) / J. Bacteriol. / Circular and linear plasmids of Lyme disease spirochetes share extensive homology: characterization of a repeated DNA element by Zuckert W. R. (1996)

Dates

Type	When
Created	8 years, 9 months ago (Nov. 10, 2016, 7:32 a.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:56 p.m.)
Indexed	1 year, 1 month ago (July 25, 2024, 12:34 a.m.)
Issued	29 years, 3 months ago (June 1, 1996)
Published	29 years, 3 months ago (June 1, 1996)
Published Print	29 years, 3 months ago (June 1, 1996)

Funders 0

None

BibTeX

@article{Porcella_1996, title={Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family}, volume={178}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.178.11.3293-3307.1996}, DOI={10.1128/jb.178.11.3293-3307.1996}, number={11}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Porcella, S F and Popova, T G and Akins, D R and Li, M and Radolf, J D and Norgard, M V}, year={1996}, month=jun, pages={3293–3307} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        7,
        25
      ]
    ],
    "date-time": "2024-07-25T04:34:10Z",
    "timestamp": 1721882050357
  },
  "reference-count": 54,
  "publisher": "American Society for Microbiology",
  "issue": "11",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1996,
            6,
            1
          ]
        ],
        "date-time": "1996-06-01T00:00:00Z",
        "timestamp": 833587200000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1996,
        6
      ]
    ]
  },
  "abstract": "<jats:p>DNA sequencing and Southern blot analyses of a Borrelia burgdorferi DNA fragment encoding a signal sequence led to the discovery of a genetic locus, designated 2.9, which appears to be present in at least seven copies in virulent B. burgdorferi 297. DNA sequence analysis of these regions revealed that each 2.9 locus contained an operon of four genes (ABCD) and open reading frames designated rep+ (positive strand) and rep- (negative strand) which encoded multiple repeat motifs. Downstream of the rep+ gene(s) in six of the completely cloned and sequenced 2.9 loci also were lipoprotein (LP) genes possessing highly similar signal sequences but encoding variable mature polypeptides. The lipoproteins could he separated into two classes on the basis of hydrophilicity profiles, sequence similarities, and reactivity with specific antibodies. The 2.9 loci were localized to two (20- and 30-kb) supercoiled plasmids in B. burgdorferi 297. Northern (RNA) blot analysis established that the 2.9 ABCD operon was only minimally expressed, whereas the rep- gene(s) and at least three of the seven LP genes were expressed by B. burgdorferi in vitro. A single putative promoter element was identified by RNA primer extension analysis upstream of the ABCD operon, whereas a number of potential promoter regions existed upstream of the LP genes. The combined data indicate that the ABCD operon, rep+ and rep- genes, and LP genes are separately transcribed during in vitro growth. The 2.9 loci possess a repetitiveness, diversity, and complexity not previously described for B. burgdorferi; differential expression of these genes may facilitate the spirochete's ability to survive in diverse host environments.</jats:p>",
  "DOI": "10.1128/jb.178.11.3293-3307.1996",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2016,
        11,
        10
      ]
    ],
    "date-time": "2016-11-10T12:32:59Z",
    "timestamp": 1478781179000
  },
  "page": "3293-3307",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 73,
  "title": "Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family",
  "prefix": "10.1128",
  "volume": "178",
  "author": [
    {
      "given": "S F",
      "family": "Porcella",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, 75235, USA."
        }
      ]
    },
    {
      "given": "T G",
      "family": "Popova",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, 75235, USA."
        }
      ]
    },
    {
      "given": "D R",
      "family": "Akins",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, 75235, USA."
        }
      ]
    },
    {
      "given": "M",
      "family": "Li",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, 75235, USA."
        }
      ]
    },
    {
      "given": "J D",
      "family": "Radolf",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, 75235, USA."
        }
      ]
    },
    {
      "given": "M V",
      "family": "Norgard",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, 75235, USA."
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "p_1",
      "unstructured": "Akins D. R. S. F. Porcella M. V. Norgard and J. D. Radolf. 1996. Unpublished observations."
    },
    {
      "key": "p_2",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1111/j.1365-2958.1995.mmi_18030507.x",
      "article-title": "Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homolog",
      "volume": "18",
      "author": "Akins D. R.",
      "year": "1995",
      "unstructured": "Akins , D. R. , S. F. Porcella , T. G. Popova , D. Shevchenko , S. I. Baker , M. Li , M. V. Norgard , and J. D. Radolf . 1995 . Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homolog . Mol. Microbiol. 18 : 507 - 520 .",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "p_3",
      "doi-asserted-by": "crossref",
      "first-page": "75",
      "DOI": "10.1111/j.1574-6968.1994.tb07204.x",
      "article-title": "Cloning and DNA sequence analysis of bmpC, a gene encoding a potential membrane lipoprotein of Borrelia burgdorferi",
      "volume": "123",
      "author": "Aron L.",
      "year": "1994",
      "unstructured": "Aron , L. , M. Alekshun , L. Perlee , I. Schwartz , H. P. Godfrey , and F. C. Cabello . 1994 . Cloning and DNA sequence analysis of bmpC, a gene encoding a potential membrane lipoprotein of Borrelia burgdorferi . FEMS Microbiol. Lett. 123 : 75 - 82 .",
      "journal-title": "FEMS Microbiol. Lett."
    },
    {
      "key": "p_4",
      "first-page": "521",
      "article-title": "Isolation and cultivation of Lyme disease spirochetes",
      "volume": "57",
      "author": "Barbour A. G.",
      "year": "1984",
      "unstructured": "Barbour , A. G. 1984 . Isolation and cultivation of Lyme disease spirochetes . Yale J. Biol. Med. 57 : 521 - 525 .",
      "journal-title": "Yale J. Biol. Med."
    },
    {
      "key": "p_5",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1128/jcm.26.3.475-478.1988",
      "article-title": "Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent",
      "volume": "26",
      "author": "Barbour A. G.",
      "year": "1988",
      "unstructured": "Barbour , A. G. 1988 . Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent . J. Clin. Microbiol. 26 : 475 - 478 .",
      "journal-title": "J. Clin. Microbiol."
    },
    {
      "key": "p_6",
      "doi-asserted-by": "crossref",
      "first-page": "155",
      "DOI": "10.1146/annurev.mi.44.100190.001103",
      "article-title": "Antigenic variation of a relapsing fever Borrelia species. Annu",
      "volume": "44",
      "author": "Barbour A. G.",
      "year": "1990",
      "unstructured": "Barbour , A. G. 1990 . Antigenic variation of a relapsing fever Borrelia species. Annu . Rev. Microbiol. 44 : 155 - 171 .",
      "journal-title": "Rev. Microbiol."
    },
    {
      "key": "p_7",
      "doi-asserted-by": "crossref",
      "first-page": "479",
      "DOI": "10.1111/j.1365-2958.1989.tb00194.x",
      "article-title": "Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochaete Borrelia burgdorferi",
      "volume": "3",
      "author": "Bergstrom S.",
      "year": "1989",
      "unstructured": "Bergstrom , S. , V. G. Bundoc , and A. G. Barbour . 1989 . Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochaete Borrelia burgdorferi . Mol. Microbiol. 3 : 479 - 486 .",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "p_8",
      "doi-asserted-by": "crossref",
      "first-page": "983",
      "DOI": "10.1128/iai.58.4.983-991.1990",
      "article-title": "Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins",
      "volume": "58",
      "author": "Brandt M. E.",
      "year": "1990",
      "unstructured": "Brandt , M. E. , B. S. Riley , J. D. Radolf , and M. V. Norgard . 1990 . Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins . Infect. Immun. 58 : 983 - 991 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_9",
      "doi-asserted-by": "crossref",
      "first-page": "2733",
      "DOI": "10.1128/IAI.57.9.2733-2741.1989",
      "article-title": "Clonal polymorphisms of outer membrane protein OspB of Borrelia burgdorferi",
      "volume": "57",
      "author": "Bundoc V. G.",
      "year": "1989",
      "unstructured": "Bundoc , V. G. , and A. G. Barbour . 1989 . Clonal polymorphisms of outer membrane protein OspB of Borrelia burgdorferi . Infect. Immun. 57 : 2733 - 2741 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_10",
      "first-page": "345",
      "article-title": "Lyme disease-United States, 1991-1992",
      "volume": "42",
      "author": "Centers for Disease Control.",
      "year": "1993",
      "unstructured": "Centers for Disease Control. 1993 . Lyme disease-United States, 1991-1992 . Morbid. Mortal. Weekly Rep. 42 : 345 - 348 .",
      "journal-title": "Morbid. Mortal. Weekly Rep."
    },
    {
      "key": "p_11",
      "doi-asserted-by": "crossref",
      "first-page": "2653",
      "DOI": "10.1128/IAI.62.7.2653-2661.1994",
      "article-title": "A 9.0-kilobase-pair circular plasmid of Borrelia burgdorferi encodes an exported protein: evidence for expression only during infection",
      "volume": "62",
      "author": "Champion C. I.",
      "year": "1994",
      "unstructured": "Champion , C. I. , D. R. Blanco , J. T. Skare , D. A. Haake , M. Giladi , D. Foley , J. N. Miller , and M. A. Lovett . 1994 . A 9.0-kilobase-pair circular plasmid of Borrelia burgdorferi encodes an exported protein: evidence for expression only during infection . Infect. Immun. 62 : 2653 - 2661 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_12",
      "doi-asserted-by": "crossref",
      "first-page": "387",
      "DOI": "10.1093/nar/12.1Part1.387",
      "article-title": "A comprehensive set of sequence analysis programs for the VAX",
      "volume": "12",
      "author": "Devereux J.",
      "year": "1984",
      "unstructured": "Devereux , J. , P. Haeberli , and O. Smithies . 1984 . A comprehensive set of sequence analysis programs for the VAX . Nucleic Acids Res. 12 : 387 - 395 .",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_13",
      "doi-asserted-by": "crossref",
      "first-page": "2706",
      "DOI": "10.1128/JB.176.9.2706-2717.1994",
      "article-title": "Complete nucleotide sequence of a circular plasmid from the Lyme disease spirochete, Borrelia burgdorferi",
      "volume": "176",
      "author": "Dunn J. J.",
      "year": "1994",
      "unstructured": "Dunn , J. J. , S. R. Buchstein , L. -L. Butler , S. Fisenne , D. S. Polin , B. N. Lade , and B. J. Luft . 1994 . Complete nucleotide sequence of a circular plasmid from the Lyme disease spirochete, Borrelia burgdorferi . J. Bacteriol. 176 : 2706 - 2717 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_14",
      "doi-asserted-by": "crossref",
      "first-page": "419",
      "DOI": "10.1128/JCM.33.2.419-427.1995",
      "article-title": "Immunoblot interpretation criteria for serodiagnosis of early Lyme disease",
      "volume": "33",
      "author": "Engstrom S. E.",
      "year": "1995",
      "unstructured": "Engstrom , S. E. , E. Shoop , and R. C. Johnson . 1995 . Immunoblot interpretation criteria for serodiagnosis of early Lyme disease . J. Clin. Microbiol. 33 : 419 - 427 .",
      "journal-title": "J. Clin. Microbiol."
    },
    {
      "key": "p_15",
      "doi-asserted-by": "crossref",
      "first-page": "5969",
      "DOI": "10.1073/pnas.86.15.5969",
      "article-title": "Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent",
      "volume": "86",
      "author": "Ferdows M. S.",
      "year": "1989",
      "unstructured": "Ferdows , M. S. , and A. G. Barbour . 1989 . Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent . Proc. Natl. Acad. Sci. USA 86 : 5969 - 5973 .",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_16",
      "doi-asserted-by": "crossref",
      "first-page": "503",
      "DOI": "10.1111/j.1365-2958.1992.tb01495.x",
      "article-title": "Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22kDa protein (pC) in Escherichia coli",
      "volume": "6",
      "author": "Fuchs R.",
      "year": "1992",
      "unstructured": "Fuchs , R. , S. Jauris , F. Lottspeich , V. Preac-Mursic , B. Wilske , and E. Soutschek . 1992 . Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22kDa protein (pC) in Escherichia coli . Mol. Microbiol. 6 : 503 - 509 .",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "p_17",
      "doi-asserted-by": "crossref",
      "first-page": "691",
      "DOI": "10.1002/ana.410370602",
      "article-title": "Lyme neuroborreliosis",
      "volume": "37",
      "author": "Garcia-Monco J. C.",
      "year": "1995",
      "unstructured": "Garcia-Monco , J. C. , and J. L. Benach . 1995 . Lyme neuroborreliosis . Ann. Neurol. 37 : 691 - 702 .",
      "journal-title": "Ann. Neurol."
    },
    {
      "key": "p_18",
      "doi-asserted-by": "crossref",
      "first-page": "3590",
      "DOI": "10.1093/nar/17.9.3590",
      "article-title": "Nucleotide sequence of a gene encoding the Borrelia burgdorferi flagellin",
      "volume": "17",
      "author": "Gassmann G. S.",
      "year": "1989",
      "unstructured": "Gassmann , G. S. , M. Kramer , U. B. Gobel , and R. Wallich . 1989 . Nucleotide sequence of a gene encoding the Borrelia burgdorferi flagellin . Nucleic Acids Res. 17 : 3590 .",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_19",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1099/00222615-36-4-229",
      "article-title": "Adherence and entry of Borrelia burgdorferi in Vero cells",
      "volume": "36",
      "author": "Hechemy K. E.",
      "year": "1992",
      "unstructured": "Hechemy , K. E. , W. A. Samsonoff , H. L. Harris , and M. McKee . 1992 . Adherence and entry of Borrelia burgdorferi in Vero cells . J. Med. Microbiol. 36 : 229 - 238 .",
      "journal-title": "J. Med. Microbiol."
    },
    {
      "key": "p_20",
      "doi-asserted-by": "crossref",
      "first-page": "5107",
      "DOI": "10.1073/pnas.82.15.5107",
      "article-title": "Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion",
      "volume": "82",
      "author": "Hoffman C. S.",
      "year": "1985",
      "unstructured": "Hoffman , C. S. , and A. Wright . 1985 . Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion . Proc. Natl. Acad. Sci. USA 82 : 5107 - 5111 .",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_21",
      "doi-asserted-by": "crossref",
      "first-page": "1321",
      "DOI": "10.1099/13500872-141-6-1321",
      "article-title": "Transcriptional and translational regulation of the expression of the major outer surface proteins in Lyme disease Borrelia strains",
      "volume": "141",
      "author": "Jonsson M.",
      "year": "1995",
      "unstructured": "Jonsson , M. , and S. Bergstrom . 1995 . Transcriptional and translational regulation of the expression of the major outer surface proteins in Lyme disease Borrelia strains . Microbiology 141 : 1321 - 1329 .",
      "journal-title": "Microbiology"
    },
    {
      "key": "p_22",
      "doi-asserted-by": "crossref",
      "first-page": "9109",
      "DOI": "10.1073/pnas.86.23.9109",
      "article-title": "Genetic evidence that RNA polymerase associated with sigma A factor uses a sporulation-specific promoter in Bacillus subtilis",
      "volume": "86",
      "author": "Kenney T. J.",
      "year": "1989",
      "unstructured": "Kenney , T. J. , K. York , P. Youngman , and C. P. Moran , Jr. 1989 . Genetic evidence that RNA polymerase associated with sigma A factor uses a sporulation-specific promoter in Bacillus subtilis . Proc. Natl. Acad. Sci. USA 86 : 9109 - 9113 .",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_23",
      "doi-asserted-by": "crossref",
      "first-page": "586",
      "DOI": "10.1093/jmedent/30.3.586",
      "article-title": "Adhesion to and invasion of cultured tick (Acarina: Ixodidae) cells by Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) and maintenance of infectivity",
      "volume": "30",
      "author": "Kurtti T. J.",
      "year": "1993",
      "unstructured": "Kurtti , T. J. , U. G. Munderloh , D. E. Krueger , R. C. Johnson , and T. G. Schwan . 1993 . Adhesion to and invasion of cultured tick (Acarina: Ixodidae) cells by Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) and maintenance of infectivity . J. Med. Entomol. 30 : 586 - 596 .",
      "journal-title": "J. Med. Entomol."
    },
    {
      "key": "p_24",
      "doi-asserted-by": "crossref",
      "first-page": "290",
      "DOI": "10.1128/IAI.62.1.290-298.1994",
      "article-title": "Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease",
      "volume": "62",
      "author": "Lam T. T.",
      "year": "1994",
      "unstructured": "Lam , T. T. , T. P. K. Nguyen , R. R. Montgomery , F. S. Kantor , E. Fikrig , and R. A. Flavell . 1994 . Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease . Infect. Immun. 62 : 290 - 298 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_25",
      "doi-asserted-by": "crossref",
      "first-page": "587",
      "DOI": "10.1146/annurev.en.36.010191.003103",
      "article-title": "Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and",
      "volume": "36",
      "author": "Lane R. S.",
      "year": "1991",
      "unstructured": "Lane , R. S. , J. Piesman , and W. Burgdorfer . 1991 . Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu. Rev. Entomol. 36 : 587 - 609 .",
      "journal-title": "Europe. Annu. Rev. Entomol."
    },
    {
      "key": "p_26",
      "doi-asserted-by": "crossref",
      "first-page": "589",
      "DOI": "10.1128/JCM.33.3.589-595.1995",
      "article-title": "Molecular typing of Borrelia burgdorferi sensu lato by PCR-restriction fragment length polymorphism analysis",
      "volume": "33",
      "author": "Liveris D.",
      "year": "1995",
      "unstructured": "Liveris , D. , A. Gazumyan , and I. Schwartz . 1995 . Molecular typing of Borrelia burgdorferi sensu lato by PCR-restriction fragment length polymorphism analysis . J. Clin. Microbiol. 33 : 589 - 595 .",
      "journal-title": "J. Clin. Microbiol."
    },
    {
      "key": "p_27",
      "doi-asserted-by": "crossref",
      "first-page": "1438",
      "DOI": "10.1056/NEJM199011223232102",
      "article-title": "Chronic neurologic manifestations of Lyme disease",
      "volume": "323",
      "author": "Logigian E. L.",
      "year": "1990",
      "unstructured": "Logigian , E. L. , R. F. Kaplan , and A. C. Steere . 1990 . Chronic neurologic manifestations of Lyme disease . N. Engl. J. Med. 323 : 1438 - 1444 .",
      "journal-title": "N. Engl. J. Med."
    },
    {
      "key": "p_28",
      "doi-asserted-by": "crossref",
      "first-page": "6427",
      "DOI": "10.1128/JB.176.21.6427-6432.1994",
      "article-title": "Plasmid location of Borrelia purine biosynthesis gene homologs",
      "volume": "176",
      "author": "Margolis N.",
      "year": "1994",
      "unstructured": "Margolis , N. , D. Hogan , K. Tilly , and P. A. Rosa . 1994 . Plasmid location of Borrelia purine biosynthesis gene homologs . J. Bacteriol. 176 : 6427 - 6432 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_29",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.4269/ajtmh.1990.43.87",
      "article-title": "Lyme borreliosis in laboratory animals: effect of host species and in vitro passage of Borrelia burgdorferi",
      "volume": "43",
      "author": "Moody K. D.",
      "year": "1990",
      "unstructured": "Moody , K. D. , S. W. Barthold , and G. A. Terwilliger . 1990 . Lyme borreliosis in laboratory animals: effect of host species and in vitro passage of Borrelia burgdorferi . Am. J. Trop. Med. Hyg. 43 : 87 - 92 .",
      "journal-title": "Am. J. Trop. Med. Hyg."
    },
    {
      "key": "p_30",
      "doi-asserted-by": "crossref",
      "first-page": "789",
      "DOI": "10.1093/nar/12.1Part2.789",
      "article-title": "Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity",
      "volume": "12",
      "author": "Mulligan M. E.",
      "year": "1984",
      "unstructured": "Mulligan , M. E. , D. K. Hawley , R. Entriken , and W. R. McClure . 1984 . Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity . Nucleic Acids Res. 12 : 789 - 800 .",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_31",
      "doi-asserted-by": "crossref",
      "first-page": "195",
      "DOI": "10.1111/j.1365-2583.1993.tb00092.x",
      "article-title": "Plasmid modifications in a tick-borne pathogen, Borrelia burgdorferi, cocultured with tick cells",
      "volume": "1",
      "author": "Munderloh U. G.",
      "year": "1993",
      "unstructured": "Munderloh , U. G. , Y. -J. Park , J. M. Dioh , A. M. Fallon , and T. J. Kurtti . 1993 . Plasmid modifications in a tick-borne pathogen, Borrelia burgdorferi, cocultured with tick cells . Insect Mol. Biol. 1 : 195 - 203 .",
      "journal-title": "Insect Mol. Biol."
    },
    {
      "key": "p_32",
      "doi-asserted-by": "crossref",
      "first-page": "4662",
      "DOI": "10.1128/IAI.60.11.4662-4672.1992",
      "article-title": "Lowpassage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein",
      "volume": "60",
      "author": "Norris S. J.",
      "year": "1992",
      "unstructured": "Norris , S. J. , C. J. Carter , J. K. Howell , and A. G. Barbour . 1992 . Lowpassage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein . Infect. Immun. 60 : 4662 - 4672 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_33",
      "doi-asserted-by": "crossref",
      "first-page": "2931",
      "DOI": "10.1099/13500872-140-11-2931",
      "article-title": "Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii",
      "volume": "140",
      "author": "Ojaimi C.",
      "year": "1994",
      "unstructured": "Ojaimi , C. , B. E. Davidson , I. Saint Girons , and I. G. Old . 1994 . Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii . Microbiology 140 : 2931 - 2940 .",
      "journal-title": "Microbiology"
    },
    {
      "key": "p_34",
      "unstructured": "Philipp M. T. 1996. Personal communication."
    },
    {
      "key": "p_35",
      "doi-asserted-by": "crossref",
      "first-page": "50",
      "DOI": "10.1128/mr.57.1.50-108.1993",
      "article-title": "The complete general secretory pathway in gram-negative bacteria",
      "volume": "57",
      "author": "Pugsley A. P.",
      "year": "1993",
      "unstructured": "Pugsley , A. P. 1993 . The complete general secretory pathway in gram-negative bacteria . Microbiol. Rev. 57 : 50 - 108 .",
      "journal-title": "Microbiol. Rev."
    },
    {
      "key": "p_36",
      "doi-asserted-by": "crossref",
      "first-page": "343",
      "DOI": "10.1111/j.1365-2958.1991.tb02115.x",
      "article-title": "The general proteinexport pathway is directly required for extracellular pullulanase secretion in Escherichia coli K12",
      "volume": "5",
      "author": "Pugsley A. P.",
      "year": "1991",
      "unstructured": "Pugsley , A. P. , M. G. Kornacker , and I. Poquet . 1991 . The general proteinexport pathway is directly required for extracellular pullulanase secretion in Escherichia coli K12 . Mol. Microbiol. 5 : 343 - 352 .",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "p_37",
      "doi-asserted-by": "crossref",
      "first-page": "900",
      "DOI": "10.1128/jb.170.2.900-907.1988",
      "article-title": "Suppression of ctc promoter mutations in Bacillus subtilis",
      "volume": "170",
      "author": "Ray C.",
      "year": "1988",
      "unstructured": "Ray , C. , M. Igo , W. Shafer , R. Losick , and C. P. Moran , Jr. 1988 . Suppression of ctc promoter mutations in Bacillus subtilis . J. Bacteriol. 170 : 900 - 907 .",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "p_38",
      "doi-asserted-by": "crossref",
      "first-page": "1115",
      "DOI": "10.1111/j.1365-2958.1993.tb01656.x",
      "article-title": "Isolation and analysis of a linear plasmid-located gene of Borrelia burgdorferi B29 encoding a 27kDa surface lipoprotein (P27) and its overexpression in Escherichia coli",
      "volume": "8",
      "author": "Reindl M.",
      "year": "1993",
      "unstructured": "Reindl , M. , B. Redl , and G. St\u00f6ffler . 1993 . Isolation and analysis of a linear plasmid-located gene of Borrelia burgdorferi B29 encoding a 27kDa surface lipoprotein (P27) and its overexpression in Escherichia coli . Mol. Microbiol. 8 : 1115 - 1124 .",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "p_39",
      "doi-asserted-by": "crossref",
      "first-page": "2192",
      "DOI": "10.1128/IAI.61.5.2192-2195.1993",
      "article-title": "The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid",
      "volume": "61",
      "author": "Sadziene A.",
      "year": "1993",
      "unstructured": "Sadziene , A. , B. Wilske , M. S. Ferdows , and A. G. Barbour . 1993 . The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid . Infect. Immun. 61 : 2192 - 2195 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_40",
      "doi-asserted-by": "crossref",
      "first-page": "1803",
      "DOI": "10.1099/13500872-140-8-1803",
      "article-title": "Molecular biology of the Borrelia, bacteria with linear replicons",
      "volume": "140",
      "author": "Saint Girons I.",
      "year": "1994",
      "unstructured": "Saint Girons , I. , I. G. Old , and B. E. Davidson . 1994 . Molecular biology of the Borrelia, bacteria with linear replicons . Microbiology 140 : 1803 - 1816 .",
      "journal-title": "Microbiology"
    },
    {
      "key": "p_41",
      "doi-asserted-by": "crossref",
      "first-page": "1831",
      "DOI": "10.1128/IAI.56.8.1831-1836.1988",
      "article-title": "Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation",
      "volume": "56",
      "author": "Schwan T. G.",
      "year": "1988",
      "unstructured": "Schwan , T. G. , W. Burgdorfer , and C. F. Garon . 1988 . Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation . Infect. Immun. 56 : 1831 - 1836 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_42",
      "doi-asserted-by": "crossref",
      "first-page": "2909",
      "DOI": "10.1073/pnas.92.7.2909",
      "article-title": "Induction of an outer surface protein on Borrelia burgdorferi during tick feeding",
      "volume": "92",
      "author": "Schwan T. G.",
      "year": "1995",
      "unstructured": "Schwan , T. G. , J. Piesman , W. T. Golde , M. C. Dolan , and P. A. Rosa . 1995 . Induction of an outer surface protein on Borrelia burgdorferi during tick feeding . Proc. Natl. Acad. Sci. USA 92 : 2909 - 2913 .",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_43",
      "doi-asserted-by": "crossref",
      "first-page": "3892",
      "DOI": "10.1128/IAI.61.9.3892-3900.1993",
      "article-title": "Specific adherence of Borrelia burgdorferi extracellular vesicles to human endothelial cells in culture",
      "volume": "61",
      "author": "Shoberg R. J.",
      "year": "1993",
      "unstructured": "Shoberg , R. J. , and D. D. Thomas . 1993 . Specific adherence of Borrelia burgdorferi extracellular vesicles to human endothelial cells in culture . Infect. Immun. 61 : 3892 - 3900 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_44",
      "doi-asserted-by": "crossref",
      "first-page": "381",
      "DOI": "10.1111/j.1574-6968.1994.tb06917.x",
      "article-title": "Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen",
      "volume": "119",
      "author": "Simpson W. J.",
      "year": "1994",
      "unstructured": "Simpson , W. J. , W. Cieplak , M. E. Schrumpf , A. G. Barbour , and T. G. Schwan . 1994 . Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen . FEMS Microbiol. Lett. 119 : 381 - 387 .",
      "journal-title": "FEMS Microbiol. Lett."
    },
    {
      "key": "p_45",
      "doi-asserted-by": "crossref",
      "first-page": "847",
      "DOI": "10.1128/iai.58.4.847-853.1990",
      "article-title": "Borrelia burgdorferi contains repeated DNA sequences that are species specific and plasmid associated",
      "volume": "58",
      "author": "Simpson W. J.",
      "year": "1990",
      "unstructured": "Simpson , W. J. , C. F. Garon , and T. G. Schwan . 1990 . Borrelia burgdorferi contains repeated DNA sequences that are species specific and plasmid associated . Infect. Immun. 58 : 847 - 853 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_46",
      "doi-asserted-by": "crossref",
      "first-page": "1723",
      "DOI": "10.1128/JCM.27.8.1723-1727.1989",
      "article-title": "Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents",
      "volume": "27",
      "author": "Sinsky R. J.",
      "year": "1989",
      "unstructured": "Sinsky , R. J. , and J. Piesman . 1989 . Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents . J. Clin. Microbiol. 27 : 1723 - 1727 .",
      "journal-title": "J. Clin. Microbiol."
    },
    {
      "key": "p_47",
      "doi-asserted-by": "crossref",
      "first-page": "586",
      "DOI": "10.1056/NEJM198908313210906",
      "article-title": "Lyme disease",
      "volume": "321",
      "author": "Steere A. C.",
      "year": "1989",
      "unstructured": "Steere , A. C. 1989 . Lyme disease . N. Engl. J. Med. 321 : 586 - 597 .",
      "journal-title": "N. Engl. J. Med."
    },
    {
      "key": "p_48",
      "unstructured": "Stevenson B. K. Tilly and P. A. Rosa. J. Bacteriol. in press."
    },
    {
      "key": "p_49",
      "doi-asserted-by": "crossref",
      "first-page": "4269",
      "DOI": "10.1073/pnas.92.10.4269",
      "article-title": "Borrelia burgdorferi genes selectively expressed in the infected host",
      "volume": "92",
      "author": "Suk K.",
      "year": "1995",
      "unstructured": "Suk , K. , S. Das , W. Sun , B. Jwang , S. W. Barthold , R. A. Flavell , and E. Fikrig . 1995 . Borrelia burgdorferi genes selectively expressed in the infected host . Proc. Natl. Acad. Sci. USA 92 : 4269 - 4273 .",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "p_50",
      "doi-asserted-by": "crossref",
      "first-page": "384",
      "DOI": "10.1128/IAI.58.2.384-392.1990",
      "article-title": "The 34-kilodalton membrane immunogen of Treponema pallidum is a lipoprotein",
      "volume": "58",
      "author": "Swancutt M. A.",
      "year": "1990",
      "unstructured": "Swancutt , M. A. , J. D. Radolf , and M. V. Norgard . 1990 . The 34-kilodalton membrane immunogen of Treponema pallidum is a lipoprotein . Infect. Immun. 58 : 384 - 392 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_51",
      "doi-asserted-by": "crossref",
      "first-page": "3314",
      "DOI": "10.1128/IAI.57.11.3314-3323.1989",
      "article-title": "Molecular characterization of the pathogen-specific 34-kilodalton membrane immunogen of Treponema pallidum",
      "volume": "57",
      "author": "Swancutt M. A.",
      "year": "1989",
      "unstructured": "Swancutt , M. A. , B. S. Riley , J. D. Radolf , and M. V. Norgard . 1989 . Molecular characterization of the pathogen-specific 34-kilodalton membrane immunogen of Treponema pallidum . Infect. Immun. 57 : 3314 - 3323 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_52",
      "doi-asserted-by": "crossref",
      "first-page": "3327",
      "DOI": "10.1128/IAI.63.9.3327-3335.1995",
      "article-title": "Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo",
      "volume": "63",
      "author": "Wallich R.",
      "year": "1995",
      "unstructured": "Wallich , R. , C. Brenner , M. D. Kramer , and M. M. Simon . 1995 . Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo . Infect. Immun. 63 : 3327 - 3335 .",
      "journal-title": "Infect. Immun."
    },
    {
      "key": "p_53",
      "doi-asserted-by": "crossref",
      "unstructured": "Zuckert W. R. E. Filipuzzi-Jenny M. Stalhammar-Carlemalm J. Melster-Turner and J. Meyer. 1994. Repeated DNA sequences on circular and linear plasmids of Borrelia burgdorferi sensu lato. p. 253-260. In J. S. Axford and D. H. E. Rees (ed.) Lyme borreliosis. Plenum Press New York.",
      "DOI": "10.1007/978-1-4615-2415-1_36"
    },
    {
      "key": "p_54",
      "doi-asserted-by": "crossref",
      "first-page": "2287",
      "DOI": "10.1128/jb.178.8.2287-2298.1996",
      "article-title": "Circular and linear plasmids of Lyme disease spirochetes share extensive homology: characterization of a repeated DNA element",
      "volume": "178",
      "author": "Zuckert W. R.",
      "year": "1996",
      "unstructured": "Zuckert , W. R. , and J. Meyer . 1996 . Circular and linear plasmids of Lyme disease spirochetes share extensive homology: characterization of a repeated DNA element . J. Bacteriol. 178 : 2287 - 2298 .",
      "journal-title": "J. Bacteriol."
    }
  ],
  "container-title": "Journal of Bacteriology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/jb.178.11.3293-3307.1996",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/jb.178.11.3293-3307.1996",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        7,
        29
      ]
    ],
    "date-time": "2021-07-29T17:56:33Z",
    "timestamp": 1627581393000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/jb.178.11.3293-3307.1996"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1996,
        6
      ]
    ]
  },
  "references-count": 54,
  "journal-issue": {
    "issue": "11",
    "published-print": {
      "date-parts": [
        [
          1996,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/jb.178.11.3293-3307.1996"
  ],
  "URL": "http://dx.doi.org/10.1128/jb.178.11.3293-3307.1996",
  "relation": {},
  "ISSN": [
    "0021-9193",
    "1098-5530"
  ],
  "subject": [],
  "container-title-short": "J Bacteriol",
  "published": {
    "date-parts": [
      [
        1996,
        6
      ]
    ]
  },
  "assertion": [
    {
      "value": "2021-01-31",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}