Molecular biology of the Borrelia, bacteria with linear replicons

Girons, Isabelle Saint; Old, Iain G.; Davidson, Barrie E.

doi:10.1099/13500872-140-8-1803

Cited by 51 publications

(35 citation statements)

References 86 publications

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“…is minichromosomes (3,17). This suggestion is prompted by these observations: (i) the presence of both a linear chromosome and linear plasmids in B. burgdorferi (3,47); (ii) the siting of genes for major outer membrane proteins and of important biosynthetic genes like guaA and guaB on plasmids (36); (iii) the identical copy number for chromosomes and plasmids in the cell (14,26,32); and, as demonstrated here, (iv) the presence in the cells of linear and circular replicons as large as 180 kb, about one-fifth the size of the chromosome. It is conceivable that previously identified circular plasmids in Borrelia spp.…”

Section: Discussionmentioning

confidence: 99%

Conversion of a linear to a circular plasmid in the relapsing fever agent Borrelia hermsii

et al. 1996

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Spirochetes of the genusSpirochetes are a distinct phylum of eubacteria (41, 55). Known pathogenic members of this division are in the genera Treponema, Borrelia, and Leptospira. The genus Borrelia comprises microorganisms that are transmitted to vertebrates by hematophagous arthropods. Included in this genus are B. hermsii and B. turicatae, agents of relapsing fever in North America; B. burgdorferi sensu lato, the cause of Lyme disease; B. anserina, the agent of avian spirochetosis; and B. coriaceae, the putative agent of epidemic bovine abortion (5).The genomes of Borrelia spp., like those of many other bacteria, are composed of a chromosome and plasmids. What distinguishes the Borrelia genome from that of most other bacteria is its largely linear structure. The chromosome of B. burgdorferi is a linear duplex DNA molecule about 1 Mb in length (6,13,14,16,17). Linear plasmids ranging in size from 5 to 55 kb are present in B. burgdorferi and B. hermsii (2, 32, 43, 54); These linear plasmids carry genes for outer membrane lipoproteins, including OspA, OspB, and OspD in B. burgdorferi (3, 4) and the serotype-specifying Vmp proteins of B. hermsii (31, 43).Borrelia spp. also have circular DNA molecules, the form of extrachromosomal DNA in most bacteria (30, 51). Although these constitute only a small fraction of the Borrelia genome, circular plasmids carry what appear to be critical genes. In B. burgdorferi, these include ospC, which codes for an outer surface protein (35,46), and homologs of guaA and guaB, which code for enzymes involved in de novo purine biosynthesis (36).The structure of linear plasmids in B. burgdorferi has been the subject of detailed examination. Electron microscopic examination of the 49-kb linear plasmid of this species showed that the two strands of the duplex DNA are covalently closed at each end (4). The telomeres of the 16-and 49-kb plasmids of B. burgdorferi have been cloned, and sequence analysis of the telomeres revealed that there are short inverted repeats at their termini and that they have terminal hairpin loops (25, 28). A similar telomeric sequence was found on linear plasmids of B. hermsii, suggesting that other linear plasmids of this genus have similar structure (31). The telomeres of linear plasmids in Borrelia spp. have structural and sequence homology to those of some linear eukaryotic DNA viruses, specifically poxviruses and African swine fever virus (25).B. hermsii and B. burgdorferi have several genome equivalents arrayed along the lengths of the wavy filamentous cells (32). Linear and circular plasmids have a copy number of approximately one to two per chromosome in both B. burgdorferi and B. hermsii (14,26,32). This arrangement suggests a tight coupling of plasmid and chromosome replication and segregation in borrelias.To further understand the genetic organization of Borrelia spp., we examined the genomes of B. hermsii, B. burgdorferi, B. turicatae, and B. anserina in more detail. In the course of this characterization, we found linear double-stranded DNA molecules w...

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Section: Discussionmentioning

confidence: 99%

Conversion of a linear to a circular plasmid in the relapsing fever agent Borrelia hermsii

et al. 1996

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“…First, the currently determined small genomes are found in mycoplasma species (585 1330 kbp [1]), or spirochaete species (900-1000 kbp [7]), followed by an archaebacteria ( Methanobacterium thermoautotrophicum 1623 kbp [8]). Direct comparison with mycoplasma spp.…”

Section: Discussionmentioning

confidence: 99%

An estimation of minimal genome size required for life

Itaya

1995

FEBS Letters

132

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The number of indispensable chromosomal loci for a bacterium, Bacillus subtilis was estimated. Seventy-nine randomly selected chromosomal loci were investigated by mutagenesis. Mutation at only six loci rendered B. subtilis unable to form colonies. In contrast, mutants for the rest of the 73 loci retained the ability to form colonies. Mutant B. subtilis with multiple-fold mutations of those dispensable loci (7-, 12-or 33-fold) were not impaired in their ability to form colonies on nutritionally adequate medium, indicating that up to 33 dispensable loci were simultaneously abolished. Given the statistical analyses for the frequency of indispensable loci (6 out of 79), total indispensable genetic material would be included within about 562 kbp. The hypothetical minimum genome size lies in the range of those currently determined smallest genomes for bacteria.

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“…Spirochetes of the genus Borrelia, for example, have a predominantly linear genome that is segmented among a 950-kb linear chromosome and several linear plasmids of 15 to 200 kb (3,34). Circular supercoiled plasmids, the form typical of plasmids of other bacteria, are also present in borreliae.…”

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The bacterial nucleoid visualized by fluorescence microscopy of cells lysed within agarose: comparison of Escherichia coli and spirochetes of the genus Borrelia

Hinnebusch

Bendich

1997

J Bacteriol

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The nucleoids of Escherichia coli and the spirochetes Borrelia burgdorferi and Borrelia hermsii, agents of Lyme disease and relapsing fever, were examined by epifluorescence microscopy of bacterial cells embedded in agarose and lysed in situ with detergent and protease. The typical E. coli nucleoid was a rosette in which 20 to 50 long loops of DNA emanated from a dense node of DNA. The percentages of cells in a population having nucleoids with zero, one, two, and three nodes varied with growth rate and growth phase. The borrelia nucleoid, in contrast, was a loose network of DNA strands devoid of nodes. This nucleoid structure difference correlates with the unusual genome of Borrelia species, which consists primarily of linear replicons, including a 950-kb linear chromosome and linear plasmids. This method provides a simple, direct means to analyze the structure of the bacterial nucleoid.Advances in DNA technology have led to an era of genomic sequencing. The entire nucleotide sequences of four bacterial genomes have been determined, and others, including that of Escherichia coli, will soon follow (1). Thus, the primary structure of the bacterial genome is becoming known in complete detail. By comparison, higher-order structures of the chromosome and how these structures accommodate transcription, replication, and partition during the bacterial cell cycle remain poorly understood (41). Because of a relative paucity of visual and cytologic clues, the structure of the prokaryotic nucleoid is also poorly understood in comparison with the structure of the eukaryotic chromosome (35).Based primarily on the E. coli model, the bacterial chromosome has long been envisaged as a single large circular molecule. The E. coli chromosome consists of 4.7 Mb of DNA which, when extended, is about 1.5 mm long. Its being packaged into a cell only 2 m long mandates a highly ordered structure. Studies of the E. coli nucleoid over many years have revealed an irregularly shaped, compact structure confined to less than half of the intracellular space (23,29). During periods of rapid growth, new rounds of chromosomal replication initiate before segregation of daughter chromosomes, and nucleoid size and shape change with growth conditions (17,32,41). The DNA is negatively supercoiled in vivo, and a number of abundant small, basic nucleoid-associated proteins (sometimes referred to as histone-like proteins) are thought to be involved in DNA packaging, with additional roles in transcription, recombination, and replication (23, 29). Worcel and Burgi first showed that the E. coli chromosome is organized into independent supercoiled domains (42), a model later supported by electron microscopy and other methods (22,23,29,30,37).Recently it has become apparent that the E. coli paradigm does not apply to all bacteria (21). Spirochetes of the genus Borrelia, for example, have a predominantly linear genome that is segmented among a 950-kb linear chromosome and several linear plasmids of 15 to 200 kb (3, 34). Circular supercoiled plasmids, the form ty...

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Molecular biology of the Borrelia, bacteria with linear replicons

Cited by 51 publications

References 86 publications

Conversion of a linear to a circular plasmid in the relapsing fever agent Borrelia hermsii

Conversion of a linear to a circular plasmid in the relapsing fever agent Borrelia hermsii

An estimation of minimal genome size required for life

The bacterial nucleoid visualized by fluorescence microscopy of cells lysed within agarose: comparison of Escherichia coli and spirochetes of the genus Borrelia

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