Host adaption to the bacteriophage carrier state of Campylobacter jejuni

Research in Microbiology

Volumn 166, Issue 6, 2015, Pages 504-515

  Brathwaite, Kelly J ^a   Siringan, Patcharin ^a   Connerton, Phillippa L ^a   Connerton, Ian F ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Bacteriophage; Campylobacter; Carrier state life cycle; RNA seq

Indexed keywords

FLAGELLIN; PHOSPHOGLYCERATE KINASE; BACTERIAL PROTEIN; FLAA PROTEIN, BACTERIA; HEAT SHOCK PROTEIN; HSPR PROTEIN, BACTERIA; REPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIOPHAGE; CAMPYLOBACTER JEJUNI; CRISPR CAS SYSTEM; GENE EXPRESSION; INTESTINE EPITHELIUM CELL; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; WILD TYPE; ADAPTATION; DOWN REGULATION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY;

CAMPYLOBACTER; CAMPYLOBACTER JEJUNI;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; BACTERIOPHAGES; CAMPYLOBACTER JEJUNI; CELL LINE, TUMOR; DOWN-REGULATION; FLAGELLIN; GENE EXPRESSION PROFILING; HEAT-SHOCK PROTEINS; HUMANS; MUTATION; PHENOTYPE; REPRESSOR PROTEINS;

EID: 84983156717     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2015.05.003     Document Type: Article

References (68)

1. Newell D.G., Elvers K.T., Dopfer D., Hansson I., Jones P., James S., et al. Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl Environ Microbiol 2011, 77:8605-8614.
2. Loc Carrillo C., Atterbury R.J., El-Shibiny A., Connerton P.L., Dillon E., Scott A., et al. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 2005, 71:6554-6563.
3. Wagenaar J.A., Van Bergen M.A., Mueller M.A., Wassenaar T.M., Carlton R.M. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 2005, 109:275-283.
4. Atterbury R.J., Connerton P.L., Dodd C.E., Rees C.E., Connerton I.F. Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl Environ Microbiol 2003, 69:6302-6306.
5. Connerton P.L., Timms A.R., Connerton I.F. Campylobacter bacteriophages and bacteriophage therapy. J Appl Microbiol 2011, 111:255-265.
6. Cairns B.J., Timms A.R., Jansen V.A., Connerton I.F., Payne R.J. Quantitative models of invitro bacteriophage-host dynamics and their application to phage therapy. PLoS Pathog 2009, 5:e1000253.
7. Javed M.A., Ackermann H.W., Azeredo J., Carvalho C.M., Connerton I., Evoy S., et al. A suggested classification for two groups of Campylobacter myoviruses. Arch Virol 2013, 159:181-190.
8. Siringan P., Connerton P.L., Payne R.J., Connerton I.F. Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms. Appl Environ Microbiol 2011, 77:3320-3326.
9. Siringan P., Connerton P.L., Cummings N.J., Connerton I.F. Alternative bacteriophage life cycles: 25 the carrier state of Campylobacter jejuni. Open Biol 2014, 4:130200.
10. Jones L.M., Mcduff C.R., Wilson J.B. Phenotypic alterations in the colonial morphology of Brucella abortus due to a bacteriophage carrier state. J Bacteriol 1962, 83:860-866.
11. Li K., Barksdale L., Garmise L. Phenotypic alterations associated with the bacteriophage carrier state of Shigella dysenteriae. J Gen Microbiol 1961, 24:355-367.
12. Coetzee J.N., Hawtrey A.O. Change in phenotype associated with the bacteriophage carrier state in a strain of Proteus mirabilis. Nature 1962, 194:1196-1197.
13. Baess I. Report on a pseudolysogenic mycobacterium and a review of the literature concerning pseudolysogeny. Acta Pathol Microbiol Scand B Microbiol Immunol 1971, 79:428-434.
14. Torsvik T., Dundas I.D. Persisting phage infection in Halobacterium salinarium str. 1. J Gen Virol 1980, 47:29-36.
15. Pauling C. Bacteriophages of Halobacterium halobium: isolated from fermented fish sauce and primary characterization. Can J Microbiol 1982, 28:916-921.
16. Jarling M., Bartkowiak K., Robenek H., Pape H., Meinhardt F. Isolation of phages infecting Actinoplanes SN223 and characterization of two of these viruses. Appl Microbiol Biotechnol 2004, 64:250-254.
17. Bastías R., Higuera G., Sierralta W., Espejo R.T. A new group of cosmopolitan bacteriophages induce a carrier state in the pandemic strain of Vibrio parahaemolyticus. Environ Microbiol 2010, 12:990-1000.
18. Lwoff A. Lysogeny. Bacteriol Rev 1953, 17:269-337.
19. Brathwaite K.J., Siringan P., Moreton J., Wilson R., Connerton I.F. Complete genome sequence of universal bacteriophage host strain Campylobacter jejuni subsp. jejuni PT14. Genome Announc 2014, 1. e00969-13.
20. Timms A.R., Cambray-Young J., Scott A.E., Petty N.K., Connerton P.L., Clarke L., et al. Evidence for a lineage of virulent bacteriophages that target Campylobacter. BMC Genomics 2010, 11:214.
21. El-Shibiny A., Scott A., Timms A., Metawea Y., Connerton P., Connerton I.F. Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Prot 2009, 72:733-740.
22. Atterbury R.J., Dillon E., Swift C., Connerton P.L., Frost J.A., Dodd C.E., et al. Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl Environ Microbiol 2005, 71:4885-4887.
23. Kirkland S.C. Dome formation by a human colonic adenocarcinoma cell line (HCA-7). Cancer Res 1985, 45:3790-3795.
24. Al-Sayeqh A.F., Loughlin M.F., Dillon E., Mellits K.H., Connerton I.F. Campylobacter jejuni activates NF-kappaB independently of TLR2, TLR4, Nod1 and Nod2 receptors. Microb Pathog 2010, 49:294-304.
25. John A., Connerton P.L., Cummings N., Connerton I.F. Profound differences in the transcriptome of Campylobacter jejuni grown in two different, widely used, microaerobic atmospheres. Res Microbiol 2011, 162:410-418.
26. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628.
27. Baggerly K., Deng L., Morris J., Aldaz C. Differential expression in SAGE: accounting for normal between-library variation. Bioinformatics 2003, 19:1477-1483.
28. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 1995, 57:289-300.
29. Krzywinski M., Schein J., Birol I., Connors J., Gascoyne R., Horsman D., et al. Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645.
30. Wassenaar T.M., Bleumink-Pluym N.M., van der Zeijst B.A. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J 1991, 10:2055-2061.
31. Novik V., Hofreuter D., Galan J.E. Identification of Campylobacter jejuni genes involved in its interaction with epithelial cells. Infect Immun 2010, 78:3540-3553. 10.1128/IAI.00109-10.
32. Holmes C.W., Penn C.W., Lund P.A. The hrcA and hspR regulons of Campylobacter jejuni. Microbiol 2010, 156:158-166. 10.1099/mic.0.031708-0.
33. Andersen M.T., Brøndsted L., Pearson B.M., Mulholland F., Parker M., Pin C., et al. Diverse roles for HspR in Campylobacter jejuni revealed by the proteome, transcriptome and phenotypic characterization of an hspR mutant. Microbiol 2005, 151:905-915. 10.1099/mic.0.27513-0.
34. Palyada K., Sun Y.Q., Flint A., Butcher J., Naikare H., Stinzi A. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. BMC Genomics 2009, 10:481. 10.1186/1471-2164-10-481.
35. Monk C.E., Pearson B.M., Mulholland F., Smith H.K., Poole R.K. Oxygen- and NssR-dependent globin expression and enhanced iron acquisition in the response of Campylobacter to nitrosative stress. J Biol Chem 2008, 283. 28413-2825. 10.1074/jbc.M801016200.
36. Makarova K.S., Haft D.H., Barrangou R., Brouns S.J., Charpentier E., Horvath P., et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011, 9:467-477. 10.1038/nrmicro2577.
37. Dugar G., Herbig A., Förstner K.U., Heidrich N., Reinhardt R., Nieselt K., et al. High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet 2013, 9:e1003495. 10.1371/journal.pgen.1003495.
38. Hooton S.P.T., Connerton I.F. Campylobacter jejuni acquire new host-derived CRISPR spacers when in association with bacteriophages harbouring a CRISPR-like Cas4 protein. Front Microbiol 2015, 5:744. 10.3389/fmicb.2014.00744.
39. Clark J.R., March J.B. Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol 2006, 24:212-218. 10.1016/j.tibtech.2006.03.003.
40. Lemak S., Beloglazova N., Nocek B., Skarina T., Flick R., Brown G., et al. Toroidal structure and DNA cleavage by the CRISPR-associated [4Fe-4S] cluster containing Cas4 nuclease SSO0001 from Sulfolobus solfataricus. J Am Chem Soc 2013, 135:17476-17487. 10.1021/ja408729b.
41. Zhang J., Kasciukovic T., White M.F. The CRISPR associated protein Cas4 is a 5' to 3' DNA exonuclease with an iron-sulfur cluster. PLoS One 2012, 7:e47232. 10.1371/journal.pone.0047232.
42. Stern A., Keren L., Wurtzel O., Amitai G., Sorek R. Self-targeting by CRISPR: gene regulation or autoimmunity?. Trends Genet 2010, 26:335-340. 10.1016/j.tig.2010.05.008.
43. Yosef I., Goren M.G., Qimron U. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 2012, 40:5569-5576. 10.1093/nar/gks216.
44. Peters J.M., Mooney R.A., Grass J.A., Jessen E.D., Tran F., Landick R. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev 2012, 26:2621-2633. 10.1101/gad.196741.112.
45. Muteeb G., Dey D., Mishra S., Sen R. A multipronged strategy of an antiterminator protein to overcome Rho-dependent transcription termination. Nucleic Acids Res 2012, 40:11213-11228. 10.1093/nar/gks872.
46. Dutta T., Malhotra A., Deutscher M.P. Exoribonuclease and endoribonuclease activities of RNase BN/RNase Z both function invivo. J Biol Chem 2012, 287:35747-35755. 10.1074/jbc.M112.407403.
47. Lertsethtakarn P., Ottemann K.M., Hendrixson D.R. Motility and chemotaxis in Campylobacter and Helicobacter. Annu Rev Microbiol 2011, 65:389-410. 10.1146/annurevmicro-090110-102908.
48. Poly F., Ewing C., Goon S., Hickey T.E., Rockabrand D., Majam G., et al. Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect Immun 2007, 75:3859-3867. 10.1128/IAI.00159-07.
49. Korolik V., Ketley J.M. Chemosensory signal transduction pathway of Campylobacter jejuni. Campylobacter 2008, 351-366. ASM Press, Washington, DC. 30 3rd ed. I. Nachamkin, C. Symanski, M.J. Blaser (Eds.).
50. Stahl M., Friis L.M., Nothaft H., Liu X., Li J., Szymanski C.M., et al. L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci USA 2011, 108:7194-7199. 10.1073/pnas.1014125108.
51. Maio J.J., Zahler S.A. Observations on the host-induced modification of T2 bacteriophage with special reference to the effects of alpha-keto acids. J Bacteriol 1958, 76:256-263.
52. Fouts D.E., Mongodin E.F., Mandrell R.E., Miller W.G., Rasko D.A., Ravel J., et al. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 2005, 3:e15. 10.1371/journal.pbio.0030015.
53. Duong T., Konkel M.E. Comparative studies of Campylobacter jejuni genomic diversity reveal the importance of core and dispensable genes in the biology of this enigmatic food-borne pathogen. Curr Opin Biotechnol 2009, 20:158-165. 10.1016/j.copbio.2009.03.004.
54. Furuta Y., Abe K., Kobayashi I. Genome comparison and context analysis reveals putative mobile forms of restriction-modification systems and related rearrangements. Nucleic Acids Res 2010, 38:2428-2443. 10.1093/nar/gkp1226.
55. Linton D., Karlyshev A.V., Wren B.W. Deciphering Campylobacter jejuni cell surface interactions from the genome sequence. Curr Opin Microbiol 2001, 4:35-40. 10.1016/S1369-5274(00)00161-2.
56. Taboada E.N., Acedillo R.R., Carrillo C.D., Findlay W.A., Medeiros D.T., Mykytczuk O.L., et al. Large-scale comparative genomics meta-analysis of Campylobacter jejuni isolates reveals low level of genome plasticity. J Clin Microbiol 2004, 42:4566-4576. 10.1128/JCM.42.10.4566-4576.2004.
57. Hiett K.L., Stintzi A., Andacht T.M., Kuntz R.L., Seal B.S. Genomic differences between Campylobacter jejuni isolates identify surface membrane and flagellar function gene products potentially important for colonizing the chicken intestine. Funct Integr Genomics 2008, 8:407-420. 10.1007/s10142-008-0087-6.
58. Bayliss C.D., Bidmos F.A., Anjum A., Manchev V.T., Richards R.L., Grossier J.P., et al. Phase variable genes of Campylobacter jejuni exhibit high mutation rates and specific mutational patterns but mutability is not the major determinant of population structure during host colonization. Nucleic Acids Res 2012, 40:5876-5889. 10.1093/nar/gks246.
59. Sørensen M.C.H., van Alphen L.B., Fodor C., Crowley S.M., Christensen B.B., Szymanski C.M., et al. Phase variable expression of capsular polysaccharide modifications allows Campylobacter jejuni to avoid bacteriophage infection in chickens. Front Cell Infect Microbiol 2012, 2:11. 10.3389/fcimb.2012.00011.
60. Coward C., Grant A.J., Swift C., Philp J., Towler R., Heydarian M., et al. Phase-variable surface structures are required for infection of Campylobacter jejuni by bacteriophages. Appl Environ Microbiol 2006, 72:4638-4647. 10.1128/AEM.00184-06.
61. Jackson R.J., Elvers K.T., Lee L.J., Gidley M.D., Wainwright L.M., Lightfoot J., et al. Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type. J Bacteriol 2007, 189:1604-1615. 10.1128/JB.00897-06.
62. Kim M., Hwang S., Ryu S., Jeon B. Regulation of perR expression by iron and PerR in Campylobacter jejuni. J Bacteriol 2011, 193:6171-6178. 10.1128/JB.05493-11.
63. Purdy D., Cawthraw S., Dickinson J.H., Newell D.G., Park S.F. Generation of a superoxide dismutase (SOD)-deficient mutant of Campylobacter coli: evidence for the significance of SOD in Campylobacter survival and colonization. Appl Environ Microbiol 1999, 65:2540-2546.
64. Atack J.M., Harvey P., Jones M.A., Kelly D.J. The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J Bacteriol 2008, 190:5279-5290. 10.1128/JB.00100-08.
65. Butcher J., Sarvan S., Brunzelle J.S., Couture J.F., Stintzi A. Structure and regulon of Campylobacter jejuni ferric uptake regulator Fur define apo-Fur regulation. Proc Natl Acad Sci U S A 2012, 109:10047-10052. 10.1073/pnas.1118321109.
66. Butcher J., Stintzi A. The transcriptional landscape of Campylobacter jejuni under iron replete and iron limited growth conditions. PLoS One 2013, 8:e79475. 10.1371/journal.pone.0079475.
67. Bucca G., Brassington A.M., Schonfeld H.J., Smith C.P. The HspR regulon of Streptomyces coelicolor: a role for the DnaK chaperone as a transcriptional co-repressor. Mol Microbiol 2000, 38:1093-1103. 10.1046/j.1365-2958.2000.02194.x.
68. Keppel F., Rychner M., Georgopoulos C. Bacteriophage-encoded cochaperonins can substitute for Escherichia coli's essential GroES protein. EMBO Rep 2002, 3:893-898. 10.1093/embo-reports/kvf176.