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Evolution of the leukotoxin promoter in genus Mannheimia.

Larsen J, Pedersen AG, Davies RL, Kuhnert P, Frey J, Christensen H, Bisgaard M, Olsen JE - BMC Evol. Biol. (2009)

Bottom Line: Transition from avirulence to virulence has occurred at least once in M. haemolytica with some evolutionary success of bovine serotype A1/A6 strains.Our analysis suggests that changes in cis-regulatory systems have contributed to the derived virulence phenotype by allowing phase-variable expression of the leukotoxin protein.We propose models for how phase shifting and the associated virulence could facilitate transmission to the nasopharynx of new hosts.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Frederiksberg C, Denmark. jesl@life.ku.dk

ABSTRACT

Background: The Mannheimia species encompass a wide variety of bacterial lifestyles, including opportunistic pathogens and commensals of the ruminant respiratory tract, commensals of the ovine rumen, and pathogens of the ruminant integument. Here we present a scenario for the evolution of the leukotoxin promoter among representatives of the five species within genus Mannheimia. We also consider how the evolution of the leukotoxin operon fits with the evolution and maintenance of virulence.

Results: The alignment of the intergenic regions upstream of the leukotoxin genes showed significant sequence and positional conservation over a 225-bp stretch immediately proximal to the transcriptional start site of the lktC gene among all Mannheimia strains. However, in the course of the Mannheimia genome evolution, the acquisition of individual noncoding regions upstream of the conserved promoter region has occurred. The rate of evolution estimated branch by branch suggests that the conserved promoter may be affected to different extents by the types of natural selection that potentially operate in regulatory regions. Tandem repeats upstream of the core promoter were confined to M. haemolytica with a strong association between the sequence of the repeat units, the number of repeat units per promoter, and the phylogenetic history of this species.

Conclusion: The mode of evolution of the intergenic regions upstream of the leukotoxin genes appears to be highly dependent on the lifestyle of the bacterium. Transition from avirulence to virulence has occurred at least once in M. haemolytica with some evolutionary success of bovine serotype A1/A6 strains. Our analysis suggests that changes in cis-regulatory systems have contributed to the derived virulence phenotype by allowing phase-variable expression of the leukotoxin protein. We propose models for how phase shifting and the associated virulence could facilitate transmission to the nasopharynx of new hosts.

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Evolution of the repeat sequences in M. haemolytica. Maximum-parsimony tree of the two distal repeat units from each promoter (A) and repeat tract polymorphisms (B) using M. haemolytica strains, which represent the diversity within this species based on MLEE, geographic origin, and host association. See the text for clusters I, II, and III. The green and red boxes highlight polymorphic sites that match and differ, respectively, from the consensus sequence. The number of repeat units per promoter is indicated. Sequence names contain the strain ID and abbreviations of the corresponding MLEE lineage (A, B, or C).
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Figure 3: Evolution of the repeat sequences in M. haemolytica. Maximum-parsimony tree of the two distal repeat units from each promoter (A) and repeat tract polymorphisms (B) using M. haemolytica strains, which represent the diversity within this species based on MLEE, geographic origin, and host association. See the text for clusters I, II, and III. The green and red boxes highlight polymorphic sites that match and differ, respectively, from the consensus sequence. The number of repeat units per promoter is indicated. Sequence names contain the strain ID and abbreviations of the corresponding MLEE lineage (A, B, or C).

Mentions: The phylogenetic tree of the distal two repeat units from M. haemolytica showed a strong association between the sequence of the repeat units, the number of repeat units per promoter, and the phylogenetic history of this species (Figure 3). First, repeat tracts containing three or more repeat units were restricted to MLEE lineage A as described above and belonged to a cluster (I) of perfect repeat units. Second, repeat tracts containing two repeat units were localised in two clusters (II and III) according to the number of repeat units that varied from the consensus sequence (one and two, respectively) and to the MLEE lineage (B and C, respectively) (Figure 3). These observations are consistent with the generally accepted view that tandem arrays of perfect repeats, such as those present in M. haemolytica strains belonging to MLEE lineage A, are hotspots for replication errors, resulting in high rates of expansions/contractions.


Evolution of the leukotoxin promoter in genus Mannheimia.

Larsen J, Pedersen AG, Davies RL, Kuhnert P, Frey J, Christensen H, Bisgaard M, Olsen JE - BMC Evol. Biol. (2009)

Evolution of the repeat sequences in M. haemolytica. Maximum-parsimony tree of the two distal repeat units from each promoter (A) and repeat tract polymorphisms (B) using M. haemolytica strains, which represent the diversity within this species based on MLEE, geographic origin, and host association. See the text for clusters I, II, and III. The green and red boxes highlight polymorphic sites that match and differ, respectively, from the consensus sequence. The number of repeat units per promoter is indicated. Sequence names contain the strain ID and abbreviations of the corresponding MLEE lineage (A, B, or C).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2697988&req=5

Figure 3: Evolution of the repeat sequences in M. haemolytica. Maximum-parsimony tree of the two distal repeat units from each promoter (A) and repeat tract polymorphisms (B) using M. haemolytica strains, which represent the diversity within this species based on MLEE, geographic origin, and host association. See the text for clusters I, II, and III. The green and red boxes highlight polymorphic sites that match and differ, respectively, from the consensus sequence. The number of repeat units per promoter is indicated. Sequence names contain the strain ID and abbreviations of the corresponding MLEE lineage (A, B, or C).
Mentions: The phylogenetic tree of the distal two repeat units from M. haemolytica showed a strong association between the sequence of the repeat units, the number of repeat units per promoter, and the phylogenetic history of this species (Figure 3). First, repeat tracts containing three or more repeat units were restricted to MLEE lineage A as described above and belonged to a cluster (I) of perfect repeat units. Second, repeat tracts containing two repeat units were localised in two clusters (II and III) according to the number of repeat units that varied from the consensus sequence (one and two, respectively) and to the MLEE lineage (B and C, respectively) (Figure 3). These observations are consistent with the generally accepted view that tandem arrays of perfect repeats, such as those present in M. haemolytica strains belonging to MLEE lineage A, are hotspots for replication errors, resulting in high rates of expansions/contractions.

Bottom Line: Transition from avirulence to virulence has occurred at least once in M. haemolytica with some evolutionary success of bovine serotype A1/A6 strains.Our analysis suggests that changes in cis-regulatory systems have contributed to the derived virulence phenotype by allowing phase-variable expression of the leukotoxin protein.We propose models for how phase shifting and the associated virulence could facilitate transmission to the nasopharynx of new hosts.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Frederiksberg C, Denmark. jesl@life.ku.dk

ABSTRACT

Background: The Mannheimia species encompass a wide variety of bacterial lifestyles, including opportunistic pathogens and commensals of the ruminant respiratory tract, commensals of the ovine rumen, and pathogens of the ruminant integument. Here we present a scenario for the evolution of the leukotoxin promoter among representatives of the five species within genus Mannheimia. We also consider how the evolution of the leukotoxin operon fits with the evolution and maintenance of virulence.

Results: The alignment of the intergenic regions upstream of the leukotoxin genes showed significant sequence and positional conservation over a 225-bp stretch immediately proximal to the transcriptional start site of the lktC gene among all Mannheimia strains. However, in the course of the Mannheimia genome evolution, the acquisition of individual noncoding regions upstream of the conserved promoter region has occurred. The rate of evolution estimated branch by branch suggests that the conserved promoter may be affected to different extents by the types of natural selection that potentially operate in regulatory regions. Tandem repeats upstream of the core promoter were confined to M. haemolytica with a strong association between the sequence of the repeat units, the number of repeat units per promoter, and the phylogenetic history of this species.

Conclusion: The mode of evolution of the intergenic regions upstream of the leukotoxin genes appears to be highly dependent on the lifestyle of the bacterium. Transition from avirulence to virulence has occurred at least once in M. haemolytica with some evolutionary success of bovine serotype A1/A6 strains. Our analysis suggests that changes in cis-regulatory systems have contributed to the derived virulence phenotype by allowing phase-variable expression of the leukotoxin protein. We propose models for how phase shifting and the associated virulence could facilitate transmission to the nasopharynx of new hosts.

Show MeSH
Related in: MedlinePlus