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Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis.

Picardeau M, Bulach DM, Bouchier C, Zuerner RL, Zidane N, Wilson PJ, Creno S, Kuczek ES, Bommezzadri S, Davis JC, McGrath A, Johnson MJ, Boursaux-Eude C, Seemann T, Rouy Z, Coppel RL, Rood JI, Lajus A, Davies JK, Médigue C, Adler B - PLoS ONE (2008)

Bottom Line: Nearly one-third of the L. biflexa genes are absent in pathogenic Leptospira.We suggest that once incorporated into the L. biflexa genome, laterally transferred DNA undergoes minimal rearrangement due to physical restrictions imposed by high gene density and limited presence of transposable elements.In contrast, the genomes of pathogenic Leptospira species undergo frequent rearrangements, often involving recombination between insertion sequences.

View Article: PubMed Central - PubMed

Affiliation: Unité de Biologie des Spirochètes, Institut Pasteur, Paris, France.

ABSTRACT
Leptospira biflexa is a free-living saprophytic spirochete present in aquatic environments. We determined the genome sequence of L. biflexa, making it the first saprophytic Leptospira to be sequenced. The L. biflexa genome has 3,590 protein-coding genes distributed across three circular replicons: the major 3,604 chromosome, a smaller 278-kb replicon that also carries essential genes, and a third 74-kb replicon. Comparative sequence analysis provides evidence that L. biflexa is an excellent model for the study of Leptospira evolution; we conclude that 2052 genes (61%) represent a progenitor genome that existed before divergence of pathogenic and saprophytic Leptospira species. Comparisons of the L. biflexa genome with two pathogenic Leptospira species reveal several major findings. Nearly one-third of the L. biflexa genes are absent in pathogenic Leptospira. We suggest that once incorporated into the L. biflexa genome, laterally transferred DNA undergoes minimal rearrangement due to physical restrictions imposed by high gene density and limited presence of transposable elements. In contrast, the genomes of pathogenic Leptospira species undergo frequent rearrangements, often involving recombination between insertion sequences. Identification of genes common to the two pathogenic species, L. borgpetersenii and L. interrogans, but absent in L. biflexa, is consistent with a role for these genes in pathogenesis. Differences in environmental sensing capacities of L. biflexa, L. borgpetersenii, and L. interrogans suggest a model which postulates that loss of signal transduction functions in L. borgpetersenii has impaired its survival outside a mammalian host, whereas L. interrogans has retained environmental sensory functions that facilitate disease transmission through water.

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Circular maps of the three L. biflexa replicons.(1) the coordinates in bp beginning at 0 = oriC; (2) dark pink: genes unique to L. biflexa, not found in L. interrogans serovar Copenhageni and L. borgpetersenii serovar Hardjobovis (identity >40% over 80% of the length of the smallest protein). (3) dark purple: genes found in L. biflexa, L. interrogans and L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (4) red: genes found in L. biflexa and L. borgpetersenii, but not in L. interrogans (identity >40% over 80% of the length of the smallest protein). (5) brown : genes found in L. biflexa and L. interrogans, but not in L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (6) blue: genes found in L. biflexa and other sequenced spirochetes (Borrelia afzelii PKo, Borrelia burgdorferi, Borrelia garinii, Treponema denticola and Treponema pallidum) (identity >40% over 80% of the length of the smallest protein ). (7) The innermost ring shows GC skew; positive skew is shown in grey, and negative skew is shown in black.
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pone-0001607-g001: Circular maps of the three L. biflexa replicons.(1) the coordinates in bp beginning at 0 = oriC; (2) dark pink: genes unique to L. biflexa, not found in L. interrogans serovar Copenhageni and L. borgpetersenii serovar Hardjobovis (identity >40% over 80% of the length of the smallest protein). (3) dark purple: genes found in L. biflexa, L. interrogans and L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (4) red: genes found in L. biflexa and L. borgpetersenii, but not in L. interrogans (identity >40% over 80% of the length of the smallest protein). (5) brown : genes found in L. biflexa and L. interrogans, but not in L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (6) blue: genes found in L. biflexa and other sequenced spirochetes (Borrelia afzelii PKo, Borrelia burgdorferi, Borrelia garinii, Treponema denticola and Treponema pallidum) (identity >40% over 80% of the length of the smallest protein ). (7) The innermost ring shows GC skew; positive skew is shown in grey, and negative skew is shown in black.

Mentions: The genome of Leptospira biflexa serovar Patoc strain Patoc1 (Ames strain) consists of three replicons with a total of 3,956,086 base pairs (bp) (Figure 1). The two larger replicons share extensive similarity to the two chromosomes that comprise the genomes of L. borgpetersenii and L. interrogans and are therefore referred to as chromosome I (CI; 3,603,977 bp; GC% 38.89) and chromosome II (CII; 277,995 bp; GC% 39.27). L. biflexa possesses a third circular replicon (74,114 bp; GC% 37.47), that we designate p74, not found in the previously sequenced pathogenic Leptospira species. (The complete genomic sequences of L. biflexa serovar Patoc strain Patoc1, strains Paris and Ames, have been deposited in GenBank under the Accession Numbers: CP000777, CP000778, CP000779, CP000786, CP000787 and CP000788).


Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis.

Picardeau M, Bulach DM, Bouchier C, Zuerner RL, Zidane N, Wilson PJ, Creno S, Kuczek ES, Bommezzadri S, Davis JC, McGrath A, Johnson MJ, Boursaux-Eude C, Seemann T, Rouy Z, Coppel RL, Rood JI, Lajus A, Davies JK, Médigue C, Adler B - PLoS ONE (2008)

Circular maps of the three L. biflexa replicons.(1) the coordinates in bp beginning at 0 = oriC; (2) dark pink: genes unique to L. biflexa, not found in L. interrogans serovar Copenhageni and L. borgpetersenii serovar Hardjobovis (identity >40% over 80% of the length of the smallest protein). (3) dark purple: genes found in L. biflexa, L. interrogans and L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (4) red: genes found in L. biflexa and L. borgpetersenii, but not in L. interrogans (identity >40% over 80% of the length of the smallest protein). (5) brown : genes found in L. biflexa and L. interrogans, but not in L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (6) blue: genes found in L. biflexa and other sequenced spirochetes (Borrelia afzelii PKo, Borrelia burgdorferi, Borrelia garinii, Treponema denticola and Treponema pallidum) (identity >40% over 80% of the length of the smallest protein ). (7) The innermost ring shows GC skew; positive skew is shown in grey, and negative skew is shown in black.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2229662&req=5

pone-0001607-g001: Circular maps of the three L. biflexa replicons.(1) the coordinates in bp beginning at 0 = oriC; (2) dark pink: genes unique to L. biflexa, not found in L. interrogans serovar Copenhageni and L. borgpetersenii serovar Hardjobovis (identity >40% over 80% of the length of the smallest protein). (3) dark purple: genes found in L. biflexa, L. interrogans and L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (4) red: genes found in L. biflexa and L. borgpetersenii, but not in L. interrogans (identity >40% over 80% of the length of the smallest protein). (5) brown : genes found in L. biflexa and L. interrogans, but not in L. borgpetersenii (identity >40% over 80% of the length of the smallest protein). (6) blue: genes found in L. biflexa and other sequenced spirochetes (Borrelia afzelii PKo, Borrelia burgdorferi, Borrelia garinii, Treponema denticola and Treponema pallidum) (identity >40% over 80% of the length of the smallest protein ). (7) The innermost ring shows GC skew; positive skew is shown in grey, and negative skew is shown in black.
Mentions: The genome of Leptospira biflexa serovar Patoc strain Patoc1 (Ames strain) consists of three replicons with a total of 3,956,086 base pairs (bp) (Figure 1). The two larger replicons share extensive similarity to the two chromosomes that comprise the genomes of L. borgpetersenii and L. interrogans and are therefore referred to as chromosome I (CI; 3,603,977 bp; GC% 38.89) and chromosome II (CII; 277,995 bp; GC% 39.27). L. biflexa possesses a third circular replicon (74,114 bp; GC% 37.47), that we designate p74, not found in the previously sequenced pathogenic Leptospira species. (The complete genomic sequences of L. biflexa serovar Patoc strain Patoc1, strains Paris and Ames, have been deposited in GenBank under the Accession Numbers: CP000777, CP000778, CP000779, CP000786, CP000787 and CP000788).

Bottom Line: Nearly one-third of the L. biflexa genes are absent in pathogenic Leptospira.We suggest that once incorporated into the L. biflexa genome, laterally transferred DNA undergoes minimal rearrangement due to physical restrictions imposed by high gene density and limited presence of transposable elements.In contrast, the genomes of pathogenic Leptospira species undergo frequent rearrangements, often involving recombination between insertion sequences.

View Article: PubMed Central - PubMed

Affiliation: Unité de Biologie des Spirochètes, Institut Pasteur, Paris, France.

ABSTRACT
Leptospira biflexa is a free-living saprophytic spirochete present in aquatic environments. We determined the genome sequence of L. biflexa, making it the first saprophytic Leptospira to be sequenced. The L. biflexa genome has 3,590 protein-coding genes distributed across three circular replicons: the major 3,604 chromosome, a smaller 278-kb replicon that also carries essential genes, and a third 74-kb replicon. Comparative sequence analysis provides evidence that L. biflexa is an excellent model for the study of Leptospira evolution; we conclude that 2052 genes (61%) represent a progenitor genome that existed before divergence of pathogenic and saprophytic Leptospira species. Comparisons of the L. biflexa genome with two pathogenic Leptospira species reveal several major findings. Nearly one-third of the L. biflexa genes are absent in pathogenic Leptospira. We suggest that once incorporated into the L. biflexa genome, laterally transferred DNA undergoes minimal rearrangement due to physical restrictions imposed by high gene density and limited presence of transposable elements. In contrast, the genomes of pathogenic Leptospira species undergo frequent rearrangements, often involving recombination between insertion sequences. Identification of genes common to the two pathogenic species, L. borgpetersenii and L. interrogans, but absent in L. biflexa, is consistent with a role for these genes in pathogenesis. Differences in environmental sensing capacities of L. biflexa, L. borgpetersenii, and L. interrogans suggest a model which postulates that loss of signal transduction functions in L. borgpetersenii has impaired its survival outside a mammalian host, whereas L. interrogans has retained environmental sensory functions that facilitate disease transmission through water.

Show MeSH
Related in: MedlinePlus