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Genome biology of Actinobacillus pleuropneumoniae JL03, an isolate of serotype 3 prevalent in China.

Xu Z, Zhou Y, Li L, Zhou R, Xiao S, Wan Y, Zhang S, Wang K, Li W, Li L, Jin H, Kang M, Dalai B, Li T, Liu L, Cheng Y, Zhang L, Xu T, Zheng H, Pu S, Wang B, Gu W, Zhang XL, Zhu GF, Wang S, Zhao GP, Chen H - PLoS ONE (2008)

Bottom Line: Preliminary analysis of the genomic sequence and the functions of the encoded proteins not only confirmed the present physiological and pathological knowledge but also offered new insights into the metabolic and virulence characteristics of this important pathogen.In addition to confirming the lack of ApxI toxin, identification of a nonsense mutation in apxIVA and a 5'-proximal truncation of the flp operon deleting both its promoter and the flp1flp2tadV genes have provided convincing scenarios for the low virulence property of JL03.Comparative genomic analysis using the available sequences of other serotypes, probable strain (serotype)-specific genomic islands related to capsular polysaccharides and lipopolysaccharide O-antigen biosyntheses were identified in JL03, which provides a foundation for future research into the mechanisms of serotypic diversity of A. pleuropneumoniae.

View Article: PubMed Central - PubMed

Affiliation: Division of Animal Infectious Disease, State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, China.

ABSTRACT
Actinobacillus pleuropneumoniae is the etiologic agent of porcine contagious pleuropneumonia, a cause of considerable world wide economic losses in the swine industry. We sequenced the complete genome of A. pleuropneumoniae, JL03, an isolate of serotype 3 prevalent in China. Its genome is a single chromosome of 2,242,062 base pairs containing 2,097 predicted protein-coding sequences, six ribosomal rRNA operons, and 63 tRNA genes. Preliminary analysis of the genomic sequence and the functions of the encoded proteins not only confirmed the present physiological and pathological knowledge but also offered new insights into the metabolic and virulence characteristics of this important pathogen. We identified a full spectrum of genes related to its characteristic chemoheterotrophic catabolism of fermentation and respiration with an incomplete TCA system for anabolism. In addition to confirming the lack of ApxI toxin, identification of a nonsense mutation in apxIVA and a 5'-proximal truncation of the flp operon deleting both its promoter and the flp1flp2tadV genes have provided convincing scenarios for the low virulence property of JL03. Comparative genomic analysis using the available sequences of other serotypes, probable strain (serotype)-specific genomic islands related to capsular polysaccharides and lipopolysaccharide O-antigen biosyntheses were identified in JL03, which provides a foundation for future research into the mechanisms of serotypic diversity of A. pleuropneumoniae.

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Schematic illustration of functional assignment to genes coding for enzymes for O-antigen biosynthesis based on predicting the topology of transmembrane proteins.All the amino acid sequences are from the genomes of A. pleuropneumoniae JL03 and E. coli K12 MG1655. CDSs designated with numbers and corresponding annotations are listed below: A. wzy (APJL1490) (wbbH), encoding oligosaccharide repeat unit polymerase; B. wzx (APJL1491) (rfbX), encoding O-antigen flippase; C. wcaJ (APJL1493), encoding glycosyltransferase; D. wzz (APJL1485) (cld), encoding an O-antigen chain length determining protein.
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pone-0001450-g004: Schematic illustration of functional assignment to genes coding for enzymes for O-antigen biosynthesis based on predicting the topology of transmembrane proteins.All the amino acid sequences are from the genomes of A. pleuropneumoniae JL03 and E. coli K12 MG1655. CDSs designated with numbers and corresponding annotations are listed below: A. wzy (APJL1490) (wbbH), encoding oligosaccharide repeat unit polymerase; B. wzx (APJL1491) (rfbX), encoding O-antigen flippase; C. wcaJ (APJL1493), encoding glycosyltransferase; D. wzz (APJL1485) (cld), encoding an O-antigen chain length determining protein.

Mentions: A bacterial sugar transferase (436aa) encoded by APJL1493 shares 55% identity with Orf9 (400aa) found in A. actinomycetemcomitans [42], but only 34% identity with a sugar transferase (472aa) encoded by APL1471 of strain L20. Two proteins (encoded by APJL1487 and 1488) among the four closely linked glycosyl transferases contain a Glycos_transf_1 domain (PF00534) in their C-termini and a Glycos_transf_2 domain (PF00535) in their N-termini, respectively, both unique among Pasteurellaceae species. Gene wzz encodes a protein (370aa) bearing 45% identity with the O-antigen chain length determining protein (MHA1853, 375aa) found in M. haemolytica [18]. Although there are much sequence variabilities among the O-antigen-processing enzymes in different Gram-negative bacteria, structural conservation and stability of membrane spanning regions still indicate that they should perform similar function predicted by the numbers and loci of relevant transmembrane helices (TMHs) (Figure 4).


Genome biology of Actinobacillus pleuropneumoniae JL03, an isolate of serotype 3 prevalent in China.

Xu Z, Zhou Y, Li L, Zhou R, Xiao S, Wan Y, Zhang S, Wang K, Li W, Li L, Jin H, Kang M, Dalai B, Li T, Liu L, Cheng Y, Zhang L, Xu T, Zheng H, Pu S, Wang B, Gu W, Zhang XL, Zhu GF, Wang S, Zhao GP, Chen H - PLoS ONE (2008)

Schematic illustration of functional assignment to genes coding for enzymes for O-antigen biosynthesis based on predicting the topology of transmembrane proteins.All the amino acid sequences are from the genomes of A. pleuropneumoniae JL03 and E. coli K12 MG1655. CDSs designated with numbers and corresponding annotations are listed below: A. wzy (APJL1490) (wbbH), encoding oligosaccharide repeat unit polymerase; B. wzx (APJL1491) (rfbX), encoding O-antigen flippase; C. wcaJ (APJL1493), encoding glycosyltransferase; D. wzz (APJL1485) (cld), encoding an O-antigen chain length determining protein.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2175527&req=5

pone-0001450-g004: Schematic illustration of functional assignment to genes coding for enzymes for O-antigen biosynthesis based on predicting the topology of transmembrane proteins.All the amino acid sequences are from the genomes of A. pleuropneumoniae JL03 and E. coli K12 MG1655. CDSs designated with numbers and corresponding annotations are listed below: A. wzy (APJL1490) (wbbH), encoding oligosaccharide repeat unit polymerase; B. wzx (APJL1491) (rfbX), encoding O-antigen flippase; C. wcaJ (APJL1493), encoding glycosyltransferase; D. wzz (APJL1485) (cld), encoding an O-antigen chain length determining protein.
Mentions: A bacterial sugar transferase (436aa) encoded by APJL1493 shares 55% identity with Orf9 (400aa) found in A. actinomycetemcomitans [42], but only 34% identity with a sugar transferase (472aa) encoded by APL1471 of strain L20. Two proteins (encoded by APJL1487 and 1488) among the four closely linked glycosyl transferases contain a Glycos_transf_1 domain (PF00534) in their C-termini and a Glycos_transf_2 domain (PF00535) in their N-termini, respectively, both unique among Pasteurellaceae species. Gene wzz encodes a protein (370aa) bearing 45% identity with the O-antigen chain length determining protein (MHA1853, 375aa) found in M. haemolytica [18]. Although there are much sequence variabilities among the O-antigen-processing enzymes in different Gram-negative bacteria, structural conservation and stability of membrane spanning regions still indicate that they should perform similar function predicted by the numbers and loci of relevant transmembrane helices (TMHs) (Figure 4).

Bottom Line: Preliminary analysis of the genomic sequence and the functions of the encoded proteins not only confirmed the present physiological and pathological knowledge but also offered new insights into the metabolic and virulence characteristics of this important pathogen.In addition to confirming the lack of ApxI toxin, identification of a nonsense mutation in apxIVA and a 5'-proximal truncation of the flp operon deleting both its promoter and the flp1flp2tadV genes have provided convincing scenarios for the low virulence property of JL03.Comparative genomic analysis using the available sequences of other serotypes, probable strain (serotype)-specific genomic islands related to capsular polysaccharides and lipopolysaccharide O-antigen biosyntheses were identified in JL03, which provides a foundation for future research into the mechanisms of serotypic diversity of A. pleuropneumoniae.

View Article: PubMed Central - PubMed

Affiliation: Division of Animal Infectious Disease, State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, China.

ABSTRACT
Actinobacillus pleuropneumoniae is the etiologic agent of porcine contagious pleuropneumonia, a cause of considerable world wide economic losses in the swine industry. We sequenced the complete genome of A. pleuropneumoniae, JL03, an isolate of serotype 3 prevalent in China. Its genome is a single chromosome of 2,242,062 base pairs containing 2,097 predicted protein-coding sequences, six ribosomal rRNA operons, and 63 tRNA genes. Preliminary analysis of the genomic sequence and the functions of the encoded proteins not only confirmed the present physiological and pathological knowledge but also offered new insights into the metabolic and virulence characteristics of this important pathogen. We identified a full spectrum of genes related to its characteristic chemoheterotrophic catabolism of fermentation and respiration with an incomplete TCA system for anabolism. In addition to confirming the lack of ApxI toxin, identification of a nonsense mutation in apxIVA and a 5'-proximal truncation of the flp operon deleting both its promoter and the flp1flp2tadV genes have provided convincing scenarios for the low virulence property of JL03. Comparative genomic analysis using the available sequences of other serotypes, probable strain (serotype)-specific genomic islands related to capsular polysaccharides and lipopolysaccharide O-antigen biosyntheses were identified in JL03, which provides a foundation for future research into the mechanisms of serotypic diversity of A. pleuropneumoniae.

Show MeSH
Related in: MedlinePlus