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Erschienen in: Archives of Virology 11/2016

19.08.2016 | Original Article

Genomic and proteomic characterization of SE-I, a temperate bacteriophage infecting Erysipelothrix rhusiopathiae

verfasst von: Wentao Yuan, Yaning Zhang, Guangcao Wang, Juan Bai, Xianwei Wang, Yufeng Li, Ping Jiang

Erschienen in: Archives of Virology | Ausgabe 11/2016

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Abstract

A bacteriophage infecting pathogenic Erysipelothrix rhusiopathiae was isolated from a swine farm experiencing an outbreak of acute swine erysipelas; we designated this phage SE-I. SE-I has an icosahedral head, a long tail and a double-stranded DNA genome. The 34,997-bp genome has a GC content of 34 % and contains 43 open reading frames (ORFs) encoding packaging, structural, lysin-holin, and hypothetical proteins. Components of purified SE-I were separated using SDS-PAGE and analyzed using liquid chromatography–mass spectrometry. Nine proteins were identified, encoded by ORF9, ORF15, ORF23, ORF30, ORF31, ORF33, ORF39, ORF40 and ORF 42. A phylogenetic tree constructed based on the sequence of the large terminase subunit revealed that SE-I is closely related to Staphylococcus phages P954 and phi3396. The CHAP-domain-containing protein encoded by ORF25 was expressed in E. coli and which was able to inactivate host bacteria. SE-I was able to infect 7 of 13 E. rhusiopathiae strains, but was unable to infect Salmonella, Streptococcus suis, and Staphylococcus aureus. This is the first report of the isolation, characterization, and genomic and proteomic analysis of a temperate phage infecting E. rhusiopathiae, and it might lead to the development of new anti- E. rhusiopathiae agents.
Literatur
1.
Zurück zum Zitat Abbasifar R, Kropinski AM, Sabour PM, Chambers JR, MacKinnon J, Malig T, Griffiths MW (2014) Efficiency of bacteriophage therapy against Cronobacter sakazakii in Galleria mellonella (greater wax moth) larvae. Arch Virol 159:2253–2261CrossRefPubMed Abbasifar R, Kropinski AM, Sabour PM, Chambers JR, MacKinnon J, Malig T, Griffiths MW (2014) Efficiency of bacteriophage therapy against Cronobacter sakazakii in Galleria mellonella (greater wax moth) larvae. Arch Virol 159:2253–2261CrossRefPubMed
2.
Zurück zum Zitat Alemayehu D, Ross RP, O’Sullivan O, Coffey A, Stanton C, Fitzgerald GF, McAuliffe O (2009) Genome of a virulent bacteriophage Lb338-1 that lyses the probiotic Lactobacillus paracasei cheese strain. Gene 448:29–39CrossRefPubMed Alemayehu D, Ross RP, O’Sullivan O, Coffey A, Stanton C, Fitzgerald GF, McAuliffe O (2009) Genome of a virulent bacteriophage Lb338-1 that lyses the probiotic Lactobacillus paracasei cheese strain. Gene 448:29–39CrossRefPubMed
3.
Zurück zum Zitat Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentral Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Bateman A, Rawlings ND (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem Sci 28:234–237CrossRefPubMed Bateman A, Rawlings ND (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem Sci 28:234–237CrossRefPubMed
5.
Zurück zum Zitat Becker SC, Swift S, Korobova O, Schischkova N, Kopylov P, Donovan DM, Abaev I (2015) Lytic activity of the staphylolytic Twort phage endolysin CHAP domain is enhanced by the SH3b cell wall binding domain. FEMS Microbiol Lett 362:1–8CrossRefPubMedPubMedCentral Becker SC, Swift S, Korobova O, Schischkova N, Kopylov P, Donovan DM, Abaev I (2015) Lytic activity of the staphylolytic Twort phage endolysin CHAP domain is enhanced by the SH3b cell wall binding domain. FEMS Microbiol Lett 362:1–8CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Bender JS, Shen HG, Irwin CK, Schwartz KJ, Opriessnig T (2010) Characterization of Erysipelothrix species isolates from clinically affected pigs, environmental samples, and vaccine strains from six recent swine erysipelas outbreaks in the United States. Clin Vaccine Immunol 17:1605–1611CrossRefPubMedPubMedCentral Bender JS, Shen HG, Irwin CK, Schwartz KJ, Opriessnig T (2010) Characterization of Erysipelothrix species isolates from clinically affected pigs, environmental samples, and vaccine strains from six recent swine erysipelas outbreaks in the United States. Clin Vaccine Immunol 17:1605–1611CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Bender JS, Irwin CK, Shen H-G, Schwartz KJ, Opriessnig T (2011) Erysipelothrix spp. genotypes, serotypes, and surface protective antigen types associated with abattoir condemnations. J Vet Diagn Invest 23:139–142CrossRefPubMed Bender JS, Irwin CK, Shen H-G, Schwartz KJ, Opriessnig T (2011) Erysipelothrix spp. genotypes, serotypes, and surface protective antigen types associated with abattoir condemnations. J Vet Diagn Invest 23:139–142CrossRefPubMed
8.
9.
10.
Zurück zum Zitat Brooke CJ, Riley TV (1999) Erysipelothrix rhusiopathiae: bacteriology, epidemiology and clinical manifestations of an occupational pathogen. J Med Microbiol 48:789–799CrossRefPubMed Brooke CJ, Riley TV (1999) Erysipelothrix rhusiopathiae: bacteriology, epidemiology and clinical manifestations of an occupational pathogen. J Med Microbiol 48:789–799CrossRefPubMed
11.
Zurück zum Zitat Chaturongakul S, Ounjai P (2014) Phage-host interplay: examples from tailed phages and gram-negative bacterial pathogens. Frontiers Microbiol 5:442CrossRef Chaturongakul S, Ounjai P (2014) Phage-host interplay: examples from tailed phages and gram-negative bacterial pathogens. Frontiers Microbiol 5:442CrossRef
13.
Zurück zum Zitat Davis RW, Thomas M, Cameron J, St John TP, Scherer S, Padgett RA (1980) Rapid DNA isolations for enzymatic and hybridization analysis. Methods Enzymol 65:404–411CrossRefPubMed Davis RW, Thomas M, Cameron J, St John TP, Scherer S, Padgett RA (1980) Rapid DNA isolations for enzymatic and hybridization analysis. Methods Enzymol 65:404–411CrossRefPubMed
14.
Zurück zum Zitat Dziewit L, Oscik K, Bartosik D, Radlinska M (2014) Molecular characterization of a novel temperate Sinorhizobium bacteriophage, capital EF, Cyrillic LM21, encoding DNA methyltransferase with CcrM-like specificity. J Virol 88:13111–13124CrossRefPubMedPubMedCentral Dziewit L, Oscik K, Bartosik D, Radlinska M (2014) Molecular characterization of a novel temperate Sinorhizobium bacteriophage, capital EF, Cyrillic LM21, encoding DNA methyltransferase with CcrM-like specificity. J Virol 88:13111–13124CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Eamens GJ, Forbes WA, Djordjevic SP (2006) Characterisation of Erysipelothrix rhusiopathiae isolates from pigs associated with vaccine breakdowns. Vet Microbiol 115:329–338CrossRefPubMed Eamens GJ, Forbes WA, Djordjevic SP (2006) Characterisation of Erysipelothrix rhusiopathiae isolates from pigs associated with vaccine breakdowns. Vet Microbiol 115:329–338CrossRefPubMed
16.
Zurück zum Zitat Feiss M, Rao VB (2012) The bacteriophage DNA packaging machine. Adv Exp Med Biol 726:489–509CrossRefPubMed Feiss M, Rao VB (2012) The bacteriophage DNA packaging machine. Adv Exp Med Biol 726:489–509CrossRefPubMed
17.
Zurück zum Zitat Ford ME, Stenstrom C, Hendrix RW, Hatfull GF (1998) Mycobacteriophage TM4: genome structure and gene expression. Tuber Lung Dis 79:63–73CrossRefPubMed Ford ME, Stenstrom C, Hendrix RW, Hatfull GF (1998) Mycobacteriophage TM4: genome structure and gene expression. Tuber Lung Dis 79:63–73CrossRefPubMed
18.
Zurück zum Zitat Golkar Z, Bagasra O, Pace DG (2014) Bacteriophage therapy: a potential solution for the antibiotic resistance crisis. J Infect Dev Ctries 8:129–136CrossRefPubMed Golkar Z, Bagasra O, Pace DG (2014) Bacteriophage therapy: a potential solution for the antibiotic resistance crisis. J Infect Dev Ctries 8:129–136CrossRefPubMed
19.
Zurück zum Zitat Hatfull GF, Sarkis GJ (1993) DNA-sequence, structure and gene-expression of mycobacteriophage-L5—a phage system for mycobacterial genetics. Mol Microbiol 7:395–405CrossRefPubMed Hatfull GF, Sarkis GJ (1993) DNA-sequence, structure and gene-expression of mycobacteriophage-L5—a phage system for mycobacterial genetics. Mol Microbiol 7:395–405CrossRefPubMed
20.
Zurück zum Zitat Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248CrossRefPubMed Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248CrossRefPubMed
21.
Zurück zum Zitat Imada Y, Takase A, Kikuma R, Iwamaru Y, Akachi S, Hayakawa Y (2004) Serotyping of 800 strains of Erysipelothrix isolated from pigs affected with erysipelas and discrimination of attenuated live vaccine strain by genotyping. J Clin Microbiol 42:2121–2126CrossRefPubMedPubMedCentral Imada Y, Takase A, Kikuma R, Iwamaru Y, Akachi S, Hayakawa Y (2004) Serotyping of 800 strains of Erysipelothrix isolated from pigs affected with erysipelas and discrimination of attenuated live vaccine strain by genotyping. J Clin Microbiol 42:2121–2126CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Katsura I (1990) Mechanism of length determination in bacteriophage lambda tails. Adv Biophys 26:1–18CrossRefPubMed Katsura I (1990) Mechanism of length determination in bacteriophage lambda tails. Adv Biophys 26:1–18CrossRefPubMed
24.
Zurück zum Zitat Kenny JG, McGrath S, Fitzgerald GF, van Sinderen D (2004) Bacteriophage Tuc 2009 encodes a tail-associated cell wall-degrading activity. J Bacteriol 186:3480–3491CrossRefPubMedPubMedCentral Kenny JG, McGrath S, Fitzgerald GF, van Sinderen D (2004) Bacteriophage Tuc 2009 encodes a tail-associated cell wall-degrading activity. J Bacteriol 186:3480–3491CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMed Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMed
26.
Zurück zum Zitat Li L, Zhang Z (2014) Isolation and characterization of a virulent bacteriophage SPW specific for Staphylococcus aureus isolated from bovine mastitis of lactating dairy cattle. Mol Biol Rep 41:5829–5838CrossRefPubMed Li L, Zhang Z (2014) Isolation and characterization of a virulent bacteriophage SPW specific for Staphylococcus aureus isolated from bovine mastitis of lactating dairy cattle. Mol Biol Rep 41:5829–5838CrossRefPubMed
27.
Zurück zum Zitat Matuszewski BK, Constanzer ML, Chavez-Eng CM (2003) Strategies for the assessment of matrix effect in quantitative bioanalytical methods based on HPLC-MS/MS. Anal Chem 75:3019–3030CrossRefPubMed Matuszewski BK, Constanzer ML, Chavez-Eng CM (2003) Strategies for the assessment of matrix effect in quantitative bioanalytical methods based on HPLC-MS/MS. Anal Chem 75:3019–3030CrossRefPubMed
28.
Zurück zum Zitat Maurizi MR, Clark WP, Katayama Y, Rudikoff S, Pumphrey J, Bowers B, Gottesman S (1990) Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265:12536–12545PubMed Maurizi MR, Clark WP, Katayama Y, Rudikoff S, Pumphrey J, Bowers B, Gottesman S (1990) Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265:12536–12545PubMed
29.
Zurück zum Zitat Merabishvili M, Vandenheuvel D, Kropinski AM, Mast J, De Vos D, Verbeken G, Noben JP, Lavigne R, Vaneechoutte M, Pirnay JP (2014) Characterization of newly isolated lytic bacteriophages active against Acinetobacter baumannii. PloS One 9:e104853CrossRefPubMedPubMedCentral Merabishvili M, Vandenheuvel D, Kropinski AM, Mast J, De Vos D, Verbeken G, Noben JP, Lavigne R, Vaneechoutte M, Pirnay JP (2014) Characterization of newly isolated lytic bacteriophages active against Acinetobacter baumannii. PloS One 9:e104853CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Munsch-Alatossava P, Alatossava T (2013) The extracellular phage–host interactions involved in the bacteriophage LL-H infection of Lactobacillus delbrueckii ssp. lactis ATCC 15808. Frontiers Microbiol 4:408CrossRef Munsch-Alatossava P, Alatossava T (2013) The extracellular phage–host interactions involved in the bacteriophage LL-H infection of Lactobacillus delbrueckii ssp. lactis ATCC 15808. Frontiers Microbiol 4:408CrossRef
32.
Zurück zum Zitat Nudler E, Gottesman ME (2002) Transcription termination and anti-termination in E. coli. Genes Cells 7:755–768CrossRefPubMed Nudler E, Gottesman ME (2002) Transcription termination and anti-termination in E. coli. Genes Cells 7:755–768CrossRefPubMed
33.
Zurück zum Zitat Opriessnig T, Hoffman LJ, Harris DL, Gaul SB, Halbur PG (2004) Erysipelothrix rhusiopathiae: genetic characterization of midwest US isolates and live commercial vaccines using pulsed-field gel electrophoresis. J Vet Diagn Invest 16:101–107CrossRefPubMed Opriessnig T, Hoffman LJ, Harris DL, Gaul SB, Halbur PG (2004) Erysipelothrix rhusiopathiae: genetic characterization of midwest US isolates and live commercial vaccines using pulsed-field gel electrophoresis. J Vet Diagn Invest 16:101–107CrossRefPubMed
34.
Zurück zum Zitat Ozawa M, Yamamoto K, Kojima A, Takagi M, Takahashi T (2009) Etiological and biological characteristics of Erysipelothrix rhusiopathiae isolated between 1994 and 2001 from pigs with swine erysipelas in Japan. J Vet Med Sci 71:697–702CrossRefPubMed Ozawa M, Yamamoto K, Kojima A, Takagi M, Takahashi T (2009) Etiological and biological characteristics of Erysipelothrix rhusiopathiae isolated between 1994 and 2001 from pigs with swine erysipelas in Japan. J Vet Med Sci 71:697–702CrossRefPubMed
35.
Zurück zum Zitat Pritchard DG, Dong S, Baker JR, Engler JA (2004) The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. Microbiology 150:2079–2087CrossRefPubMed Pritchard DG, Dong S, Baker JR, Engler JA (2004) The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. Microbiology 150:2079–2087CrossRefPubMed
36.
Zurück zum Zitat Richardson JP (2002) Rho-dependent termination and ATPases in transcript termination. Biochim Biophys Acta 1577:251–260CrossRefPubMed Richardson JP (2002) Rho-dependent termination and ATPases in transcript termination. Biochim Biophys Acta 1577:251–260CrossRefPubMed
37.
Zurück zum Zitat Rigden DJ, Jedrzejas MJ, Galperin MY (2003) Amidase domains from bacterial and phage autolysins define a family of gamma-d, l-glutamate-specific amidohydrolases. Trends Biochem Sci 28:230–234CrossRefPubMed Rigden DJ, Jedrzejas MJ, Galperin MY (2003) Amidase domains from bacterial and phage autolysins define a family of gamma-d, l-glutamate-specific amidohydrolases. Trends Biochem Sci 28:230–234CrossRefPubMed
38.
Zurück zum Zitat Santos SB, Kropinski AM, Ceyssens PJ, Ackermann HW, Villegas A, Lavigne R, Krylov VN, Carvalho CM, Ferreira EC, Azeredo J (2011) Genomic and proteomic characterization of the broad-host-range Salmonella phage PVP-SE1: creation of a new phage genus. J Virol 85:11265–11273CrossRefPubMedPubMedCentral Santos SB, Kropinski AM, Ceyssens PJ, Ackermann HW, Villegas A, Lavigne R, Krylov VN, Carvalho CM, Ferreira EC, Azeredo J (2011) Genomic and proteomic characterization of the broad-host-range Salmonella phage PVP-SE1: creation of a new phage genus. J Virol 85:11265–11273CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Schouler C, Ehrlich SD, Chopin MC (1994) Sequence and organization of the lactococcal prolate-headed bIL67 phage genome. Microbiology 140(Pt 11):3061–3069CrossRefPubMed Schouler C, Ehrlich SD, Chopin MC (1994) Sequence and organization of the lactococcal prolate-headed bIL67 phage genome. Microbiology 140(Pt 11):3061–3069CrossRefPubMed
40.
Zurück zum Zitat Skurnik M, Hyytiainen HJ, Happonen LJ, Kiljunen S, Datta N, Mattinen L, Williamson K, Kristo P, Szeliga M, Kalin-Manttari L, Ahola-Iivarinen E, Kalkkinen N, Butcher SJ (2012) Characterization of the genome, proteome, and structure of yersiniophage varphiR1-37. J Virol 86:12625–12642CrossRefPubMedPubMedCentral Skurnik M, Hyytiainen HJ, Happonen LJ, Kiljunen S, Datta N, Mattinen L, Williamson K, Kristo P, Szeliga M, Kalin-Manttari L, Ahola-Iivarinen E, Kalkkinen N, Butcher SJ (2012) Characterization of the genome, proteome, and structure of yersiniophage varphiR1-37. J Virol 86:12625–12642CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Sugai M, Fujiwara T, Akiyama T, Ohara M, Komatsuzawa H, Inoue S, Suginaka H (1997) Purification and molecular characterization of glycylglycine endopeptidase produced by Staphylococcus capitis EPK1. J Bacteriol 179:1193–1202PubMedPubMedCentral Sugai M, Fujiwara T, Akiyama T, Ohara M, Komatsuzawa H, Inoue S, Suginaka H (1997) Purification and molecular characterization of glycylglycine endopeptidase produced by Staphylococcus capitis EPK1. J Bacteriol 179:1193–1202PubMedPubMedCentral
42.
Zurück zum Zitat Takahashi T, Nagamine N, Kijima M, Suzuki S, Takagi M, Tamura Y, Nakamura M, Muramatsu M, Sawada T (1996) Serovars of Erysipelothrix strains isolated from pigs affected with erysipelas in Japan. J Vet Med Sci 58:587–589CrossRefPubMed Takahashi T, Nagamine N, Kijima M, Suzuki S, Takagi M, Tamura Y, Nakamura M, Muramatsu M, Sawada T (1996) Serovars of Erysipelothrix strains isolated from pigs affected with erysipelas in Japan. J Vet Med Sci 58:587–589CrossRefPubMed
43.
Zurück zum Zitat Tegel H, Tourle S, Ottosson J, Persson A (2010) Increased levels of recombinant human proteins with the Escherichia coli strain Rosetta(DE3). Protein Expr purif 69:159–167CrossRefPubMed Tegel H, Tourle S, Ottosson J, Persson A (2010) Increased levels of recombinant human proteins with the Escherichia coli strain Rosetta(DE3). Protein Expr purif 69:159–167CrossRefPubMed
44.
Zurück zum Zitat Vegge CS, Vogensen FK, McGrath S, Neve H, van Sinderen D, Brondsted L (2006) Identification of the lower baseplate protein as the antireceptor of the temperate lactococcal bacteriophages TP901-1 and Tuc 2009. J Bacteriol 188:55–63CrossRefPubMedPubMedCentral Vegge CS, Vogensen FK, McGrath S, Neve H, van Sinderen D, Brondsted L (2006) Identification of the lower baseplate protein as the antireceptor of the temperate lactococcal bacteriophages TP901-1 and Tuc 2009. J Bacteriol 188:55–63CrossRefPubMedPubMedCentral
45.
46.
Zurück zum Zitat Wood RL, Harrington R Jr (1978) Serotypes of Erysipelothrix rhusiopathiae isolated from swine and from soil and manure of swine pens in the United States. Am J Vet Res 39:1833–1840PubMed Wood RL, Harrington R Jr (1978) Serotypes of Erysipelothrix rhusiopathiae isolated from swine and from soil and manure of swine pens in the United States. Am J Vet Res 39:1833–1840PubMed
47.
Zurück zum Zitat Wood RL (1999) Erysipelas. In: Straw BE, D’Allaire S, Mengeling ML, Taylor DJ (eds) Diseases of swine, 8th edn. Iowa State University Press, Ames, pp 419–430 Wood RL (1999) Erysipelas. In: Straw BE, D’Allaire S, Mengeling ML, Taylor DJ (eds) Diseases of swine, 8th edn. Iowa State University Press, Ames, pp 419–430
48.
Zurück zum Zitat Zou Y, Zhu X, Muhammad HM, Jiang P, Li Y (2015) Characterization of Erysipelothrix rhusiopathiae strains isolated from acute swine erysipelas outbreaks in Eastern China. J Vet Med Sci 77:653–660CrossRefPubMedPubMedCentral Zou Y, Zhu X, Muhammad HM, Jiang P, Li Y (2015) Characterization of Erysipelothrix rhusiopathiae strains isolated from acute swine erysipelas outbreaks in Eastern China. J Vet Med Sci 77:653–660CrossRefPubMedPubMedCentral
Metadaten
Titel
Genomic and proteomic characterization of SE-I, a temperate bacteriophage infecting Erysipelothrix rhusiopathiae
verfasst von
Wentao Yuan
Yaning Zhang
Guangcao Wang
Juan Bai
Xianwei Wang
Yufeng Li
Ping Jiang
Publikationsdatum
19.08.2016
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 11/2016
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-016-3018-1

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