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Molecular analysis of the leukotoxin determinants from Pasteurella haemolytica serotypes 1 to 16.

ABSTRACT: All sixteen serotypes of Pasteurella haemolytica were shown to produce a leukotoxin protein which is immunologically related to the well-characterized serotype 1 leukotoxin. All of the leukotoxins were weakly hemolytic and were able to bind to BL-3 target cells. The leukotoxin determinants were characterized by Southern blot hybridization by use of the previously cloned serotype 1 determinant as the probe, and a number of distinct classes were identified. The leukotoxin determinants from serotypes 2, 3, and 11 were cloned. Nucleotide sequence analysis of the lktC and lktA genes of the serotype 3 and 11 determinants revealed nucleotide substitutions throughout the coding sequences. A comparison of the lktC and lktA genes and deduced proteins of serotypes 1, 3, and 11 showed that they are highly homologous.

SUBMITTER: Burrows LL

PROVIDER: S-EPMC281275 | biostudies-other | 1993 Dec

REPOSITORIES: biostudies-other

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Molecular analysis of the leukotoxin determinants from Pasteurella haemolytica serotypes 1 to 16.

Burrows L L LL Olah-Winfield E E Lo R Y RY

Infection and immunity 19931201 12

All sixteen serotypes of Pasteurella haemolytica were shown to produce a leukotoxin protein which is immunologically related to the well-characterized serotype 1 leukotoxin. All of the leukotoxins were weakly hemolytic and were able to bind to BL-3 target cells. The leukotoxin determinants were characterized by Southern blot hybridization by use of the previously cloned serotype 1 determinant as the probe, and a number of distinct classes were identified. The leukotoxin determinants from serotyp ...[more]

PMID: 8225575

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Project description:The mosaic structure and molecular evolution of the leukotoxin operon (lktCABD) was investigated by nucleotide sequence comparison of the lktC, lktB, and lktD genes in 23 Mannheimia (Pasteurella) haemolytica, 6 Mannheimia glucosida, and 4 Pasteurella trehalosi strains. Sequence variation in the lktA gene has been described previously (R. L. Davies et al., J. Bacteriol. 183:1394-1404, 2001). The leukotoxin operon of M. haemolytica has a complex mosaic structure and has been derived by extensive inter- and intraspecies horizontal DNA transfer and intragenic recombination events. However, the pattern of recombination varies throughout the operon and among the different evolutionary lineages of M. haemolytica. The lktA and lktB genes have the most complex mosaic structures with segments derived from up to four different sources, including M. glucosida and P. trehalosi. In contrast, the lktD gene is highly conserved in M. haemolytica. The lktC, lktA, and lktB genes of strains representing the major ovine lineages contain recombinant segments derived from bovine or bovine-like serotype A2 strains. These findings support the previous conclusion that host switching of bovine A2 strains from cattle to sheep has played a major role in the evolution of the leukotoxin operon in ovine strains of M. haemolytica. Homologous segments of donor and recipient alleles are identical, or nearly identical, indicating that the recombinational exchanges occurred relatively recent in evolutionary terms. The 5' and 3' ends of the operon are highly conserved in M. haemolytica, which suggests that multiple horizontal exchanges of the complete operon have occurred by a common mechanism such as transduction. Although the lktA and lktB genes both have complex mosaic structures and high nucleotide substitution rates, the amino acid diversity of LktB is significantly lower than that of LktA due to a higher degree of evolutionary constraint against amino acid replacement. The recombinational exchanges within the leukotoxin operon have had greatest effect on LktA and probably provide an adaptive advantage against the host antibody response by generating novel antigenic variation at surface-exposed sites.

Project description:The molecular evolution of the leukotoxin structural gene (lktA) of Mannheimia (Pasteurella) haemolytica was investigated by nucleotide sequence comparison of lktA in 31 bovine and ovine strains representing the various evolutionary lineages and serotypes of the species. Eight major allelic variants (1.4 to 15.7% nucleotide divergence) were identified; these have mosaic structures of varying degrees of complexity reflecting a history of horizontal gene transfer and extensive intragenic recombination. The presence of identical alleles in strains of different genetic backgrounds suggests that assortative (entire gene) recombination has also contributed to strain diversification in M. haemolytica. Five allelic variants occur only in ovine strains and consist of recombinant segments derived from as many as four different sources. Four of these alleles consist of DNA (52.8 to 96.7%) derived from the lktA gene of the two related species Mannheimia glucosida and Pasteurella trehalosi, and four contain recombinant segments derived from an allele that is associated exclusively with bovine or bovine-like serotype A2 strains. The two major lineages of ovine serotype A2 strains possess lktA alleles that have very different evolutionary histories and encode divergent leukotoxins (5.3% amino acid divergence), but both contain segments derived from the bovine allele. Homologous segments of donor and recipient alleles are identical or nearly identical, indicating that the recombination events are relatively recent and probably postdate the domestication of cattle and sheep. Our findings suggest that host switching of bovine strains from cattle to sheep, together with inter- and intraspecies recombinational exchanges, has played an important role in generating leukotoxin diversity in ovine strains. In contrast, there is limited allelic diversity of lktA in bovine strains, suggesting that transmission of strains from sheep to cattle has been less important in leukotoxin evolution.

Dataset Information

Molecular analysis of the leukotoxin determinants from Pasteurella haemolytica serotypes 1 to 16.

Publications

Molecular analysis of the leukotoxin determinants from Pasteurella haemolytica serotypes 1 to 16.

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