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

Mathieu Picardeau,John K Davies,Christiane Bouchier,Annette Mcgrath,Ross L Coppel,Nora Zidane,Simona Bommezzadri,Claudine Médigue,Aurélie Lajus,Torsten Seemann,Caroline Boursaux-Eude,Zoé Rouy,Ben Adler,Richard L Zuerner,Julian I Rood,Dieter Bulach ,John D Davis ,Elizabeth Kuczek ,Matthew R Johnson ,Sophie Créno ,Peter Wilson

doi:10.1371/journal.pone.0001607

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.

Highlights

The genus Leptospira contains pathogenic and saprophytic species that differ in their capacity for survival in a vast array of environments that range from soil and water [1] to the tissues of mammalian hosts during acute and chronic infection [2]
A process of genome erosion and loss of gene function in L. borgpetersenii serovar Hardjo [5] limits its viability outside a mammalian host and likely impairs disease transmission through water, a route commonly used by L. interrogans to infect new hosts
To gain insight into the genetic potential of Leptospira and to help identify genes that contribute to long-term survival in surface water, we determined the genome sequences of two L. biflexa strains, the first saprophytic Leptospira species to be characterized by genome analysis

Summary

Introduction

The genus Leptospira contains pathogenic and saprophytic species that differ in their capacity for survival in a vast array of environments that range from soil and water [1] to the tissues of mammalian hosts during acute and chronic infection [2]. To gain insight into the genetic potential of Leptospira and to help identify genes that contribute to long-term survival in surface water, we determined the genome sequences of two L. biflexa strains, the first saprophytic Leptospira species to be characterized by genome analysis. 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).

Results

Conclusion