Limits...
Analysis of gene order data supports vertical inheritance of the leukotoxin operon and genome rearrangements in the 5' flanking region in genus Mannheimia.

Larsen J, Kuhnert P, Frey J, Christensen H, Bisgaard M, Olsen JE - BMC Evol. Biol. (2007)

Bottom Line: We examined the gene order in the 5' flanking region of the leukotoxin operon and found that the 5' flanking gene strings, hslVU-lapB-artJ-lktC and xylAB-lktC, are peculiar to M. haemolytica + M. glucosida and M. granulomatis, respectively, whereas the gene string hslVU-lapB-lktC is present in M. ruminalis, the supposed sister group of M. haemolytica + M. glucosida, and in the most ancient subclade M. varigena.In M. granulomatis, we found remnants of the gene string hslVU-lapB-lktC in the xylB-lktC intergenic region.The evolution of the novel 5' flanking region in M. haemolytica + M. glucosida resulted in transcriptional coupling between the divergently arranged artJ and lkt promoters.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Stigbøjlen 4, DK-1870 Frederiksberg C, Denmark. jesl@life.ku.dk

ABSTRACT

Background: The Mannheimia subclades belong to the same bacterial genus, but have taken divergent paths toward their distinct lifestyles. For example, M. haemolytica + M. glucosida are potential pathogens of the respiratory tract in the mammalian suborder Ruminantia, whereas M. ruminalis, the supposed sister group, lives as a commensal in the ovine rumen. We have tested the hypothesis that vertical inheritance of the leukotoxin (lktCABD) operon has occurred from the last common ancestor of genus Mannheimia to any ancestor of the diverging subclades by exploring gene order data.

Results: We examined the gene order in the 5' flanking region of the leukotoxin operon and found that the 5' flanking gene strings, hslVU-lapB-artJ-lktC and xylAB-lktC, are peculiar to M. haemolytica + M. glucosida and M. granulomatis, respectively, whereas the gene string hslVU-lapB-lktC is present in M. ruminalis, the supposed sister group of M. haemolytica + M. glucosida, and in the most ancient subclade M. varigena. In M. granulomatis, we found remnants of the gene string hslVU-lapB-lktC in the xylB-lktC intergenic region.

Conclusion: These observations indicate that the gene string hslVU-lapB-lktC is more ancient than the hslVU-lapB-artJ-lktC and xylAB-lktC gene strings. The presence of (remnants of) the ancient gene string hslVU-lapB-lktC among any subclades within genus Mannheimia supports that it has been vertically inherited from the last common ancestor of genus Mannheimia to any ancestor of the diverging subclades, thus reaffirming the hypothesis of vertical inheritance of the leukotoxin operon. The presence of individual 5' flanking regions in M. haemolytica + M. glucosida and M. granulomatis reflects later genome rearrangements within each subclade. The evolution of the novel 5' flanking region in M. haemolytica + M. glucosida resulted in transcriptional coupling between the divergently arranged artJ and lkt promoters. We propose that the chimeric promoter have led to high level expression of the leukotoxin operon which could explain the increased potential of certain M. haemolytica + M. glucosida strains to cause a particular type of infection.

Show MeSH

Related in: MedlinePlus

Evolution of the 5' flanking gene order in the Mannheimia genomes analyzed in this study. The organismal cladogram that describes bifurcation order was adapted from Larsen et al. [26]. Colored arrows indicate orthology as in Figure 2. Gene names are those reported in protein databases or have been assigned by us on the basis of orthology relationships. Pseudogenes are indicated by a "Ψ". The two types of genome rearrangements are indicated by circles. Nomenclature: sequence names contain abbreviations of the taxonomic group (genus and species) followed by the corresponding strain ID as listed in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2228313&req=5

Figure 1: Evolution of the 5' flanking gene order in the Mannheimia genomes analyzed in this study. The organismal cladogram that describes bifurcation order was adapted from Larsen et al. [26]. Colored arrows indicate orthology as in Figure 2. Gene names are those reported in protein databases or have been assigned by us on the basis of orthology relationships. Pseudogenes are indicated by a "Ψ". The two types of genome rearrangements are indicated by circles. Nomenclature: sequence names contain abbreviations of the taxonomic group (genus and species) followed by the corresponding strain ID as listed in Table 1.

Mentions: The sizes of the sequenced genome segments varied from 1,383 to 9,126 bp (Table 1). Our initial search for putative orthologs suggested that the 5' flanking gene strings, hslVU-lapB-artI/artJ-lktC and xylAB-lktC, are peculiar to M. haemolytica + M. glucosida and M. granulomatis, respectively, whereas the gene string hslVU-lapB-lktC is present in M. ruminalis, the supposed sister group of M. haemolytica + M. glucosida, and in the most ancient subclade M. varigena (Figure 1). It should be noted that for one open reading frame (ORF) we retrieved two closely related proteins, ArtI and ArtJ, in a subset of the genomes and that the corresponding artI/artJ gene is located on the opposite strand immediately upstream of the lkt operon.


Analysis of gene order data supports vertical inheritance of the leukotoxin operon and genome rearrangements in the 5' flanking region in genus Mannheimia.

Larsen J, Kuhnert P, Frey J, Christensen H, Bisgaard M, Olsen JE - BMC Evol. Biol. (2007)

Evolution of the 5' flanking gene order in the Mannheimia genomes analyzed in this study. The organismal cladogram that describes bifurcation order was adapted from Larsen et al. [26]. Colored arrows indicate orthology as in Figure 2. Gene names are those reported in protein databases or have been assigned by us on the basis of orthology relationships. Pseudogenes are indicated by a "Ψ". The two types of genome rearrangements are indicated by circles. Nomenclature: sequence names contain abbreviations of the taxonomic group (genus and species) followed by the corresponding strain ID as listed in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2228313&req=5

Figure 1: Evolution of the 5' flanking gene order in the Mannheimia genomes analyzed in this study. The organismal cladogram that describes bifurcation order was adapted from Larsen et al. [26]. Colored arrows indicate orthology as in Figure 2. Gene names are those reported in protein databases or have been assigned by us on the basis of orthology relationships. Pseudogenes are indicated by a "Ψ". The two types of genome rearrangements are indicated by circles. Nomenclature: sequence names contain abbreviations of the taxonomic group (genus and species) followed by the corresponding strain ID as listed in Table 1.
Mentions: The sizes of the sequenced genome segments varied from 1,383 to 9,126 bp (Table 1). Our initial search for putative orthologs suggested that the 5' flanking gene strings, hslVU-lapB-artI/artJ-lktC and xylAB-lktC, are peculiar to M. haemolytica + M. glucosida and M. granulomatis, respectively, whereas the gene string hslVU-lapB-lktC is present in M. ruminalis, the supposed sister group of M. haemolytica + M. glucosida, and in the most ancient subclade M. varigena (Figure 1). It should be noted that for one open reading frame (ORF) we retrieved two closely related proteins, ArtI and ArtJ, in a subset of the genomes and that the corresponding artI/artJ gene is located on the opposite strand immediately upstream of the lkt operon.

Bottom Line: We examined the gene order in the 5' flanking region of the leukotoxin operon and found that the 5' flanking gene strings, hslVU-lapB-artJ-lktC and xylAB-lktC, are peculiar to M. haemolytica + M. glucosida and M. granulomatis, respectively, whereas the gene string hslVU-lapB-lktC is present in M. ruminalis, the supposed sister group of M. haemolytica + M. glucosida, and in the most ancient subclade M. varigena.In M. granulomatis, we found remnants of the gene string hslVU-lapB-lktC in the xylB-lktC intergenic region.The evolution of the novel 5' flanking region in M. haemolytica + M. glucosida resulted in transcriptional coupling between the divergently arranged artJ and lkt promoters.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Veterinary Pathobiology, Faculty of Life Sciences, University of Copenhagen, Stigbøjlen 4, DK-1870 Frederiksberg C, Denmark. jesl@life.ku.dk

ABSTRACT

Background: The Mannheimia subclades belong to the same bacterial genus, but have taken divergent paths toward their distinct lifestyles. For example, M. haemolytica + M. glucosida are potential pathogens of the respiratory tract in the mammalian suborder Ruminantia, whereas M. ruminalis, the supposed sister group, lives as a commensal in the ovine rumen. We have tested the hypothesis that vertical inheritance of the leukotoxin (lktCABD) operon has occurred from the last common ancestor of genus Mannheimia to any ancestor of the diverging subclades by exploring gene order data.

Results: We examined the gene order in the 5' flanking region of the leukotoxin operon and found that the 5' flanking gene strings, hslVU-lapB-artJ-lktC and xylAB-lktC, are peculiar to M. haemolytica + M. glucosida and M. granulomatis, respectively, whereas the gene string hslVU-lapB-lktC is present in M. ruminalis, the supposed sister group of M. haemolytica + M. glucosida, and in the most ancient subclade M. varigena. In M. granulomatis, we found remnants of the gene string hslVU-lapB-lktC in the xylB-lktC intergenic region.

Conclusion: These observations indicate that the gene string hslVU-lapB-lktC is more ancient than the hslVU-lapB-artJ-lktC and xylAB-lktC gene strings. The presence of (remnants of) the ancient gene string hslVU-lapB-lktC among any subclades within genus Mannheimia supports that it has been vertically inherited from the last common ancestor of genus Mannheimia to any ancestor of the diverging subclades, thus reaffirming the hypothesis of vertical inheritance of the leukotoxin operon. The presence of individual 5' flanking regions in M. haemolytica + M. glucosida and M. granulomatis reflects later genome rearrangements within each subclade. The evolution of the novel 5' flanking region in M. haemolytica + M. glucosida resulted in transcriptional coupling between the divergently arranged artJ and lkt promoters. We propose that the chimeric promoter have led to high level expression of the leukotoxin operon which could explain the increased potential of certain M. haemolytica + M. glucosida strains to cause a particular type of infection.

Show MeSH
Related in: MedlinePlus