Gene loss and lineage-specific restriction-modification systems associated with niche differentiation in the Campylobacter jejuni sequence type 403 clonal complex

Applied and Environmental Microbiology

Volumn 81, Issue 11, 2015, Pages 3641-3647

  Morley, Laura ^a   McNally, Alan ^a   Paszkiewicz, Konrad ^b   Corander, Jukka ^c   Méric, Guillaume ^d   Sheppard, Samuel K ^d,e   Blom, Jochen ^f   Manning, Georgina ^a  

^a NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

^d SWANSEA UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURE; GENES;

CAMPYLOBACTER JEJUNI; CLONAL COMPLEX; CODING SEQUENCES; DIVERSE SPECIES; GENE DECAY; HUMAN DISEASE; NICHE DIFFERENTIATION; RESTRICTION-MODIFICATION SYSTEMS;

BACTERIA;

CLONE; GENE EXPRESSION; INFECTIOUS DISEASE; LIVESTOCK FARMING; MICROBIAL ACTIVITY; MUTATION; SPECIES DIVERSITY;

ANIMALIA; AVES; BOS; CAMPYLOBACTER JEJUNI; SUIDAE;

RESTRICTION ENDONUCLEASE; STOP CODON;

ANIMAL; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; CLASSIFICATION; ENZYMOLOGY; GENE DELETION; GENETIC RECOMBINATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MULTILOCUS SEQUENCE TYPING; POULTRY; STOP CODON; VETERINARY;

ANIMALS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CODON, NONSENSE; DNA RESTRICTION-MODIFICATION ENZYMES; EVOLUTION, MOLECULAR; GENE DELETION; MULTILOCUS SEQUENCE TYPING; POULTRY; RECOMBINATION, GENETIC;

EID: 84930017845     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00546-15     Document Type: Article

References (39)

1. Janssen R, Krogfelt KA, Cawthraw SA, van Pelt W, Wagenaar JA, Owen RJ. 2008. Host-pathogen interactions in Campylobacter infections: the host perspective. Clin Microbiol Rev 21:505-518. http://dx.doi.org/10.1128/CMR.00055-07.
2. Young KT, Davis LM, Dirita VJ. 2007. Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev 5:665-679. http://dx.doi.org/10.1038/nrmicro1718.
3. Gillespie I, O'Brien S, Frost J, Adak G, Horby P, Swan A, Painter M, Neal K, Campylobacter Sentinel Surveillance Scheme Collaborators. 2002. A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg Infect Dis 8:937-942. http://dx.doi.org/10.3201/eid0809.010817.
4. Sheppard SK, Dallas JF, MacRae M, McCarthy ND, Sproston EL, Gormley FJ, Strachan NJ, Ogden ID, Maiden MC, Forbes KJ. 2009. Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. Int J Food Microbiol 134:96-103. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.02.010.
5. Sheppard SK, Cheng L, Méric G, de Haan CP, Llarena AK, Marttinen P, Vidal A, Ridley A, Clifton-Hadley F, Connor TR, Strachan NJ, Forbes K, Colles FM, Jolley KA, Bentley SD, Maiden MC, Hänninen ML, Parkhill J, Hanage WP, Corander J. 2014. Cryptic ecology among host generalist Campylobacter jejuni in domestic animals. Mol Ecol 23: 2442-2451. http://dx.doi.org/10.1111/mec.12742.
6. Strachan NJ, MacRae M, Thomson A, Rotariu O, Ogden ID, Forbes KJ. 2012. Source attribution, prevalence and enumeration of Campylobacter spp. from retail liver. Int J Food Microbiol 153:234-236. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.10.033.
7. Strachan NJ, Gormley FJ, Rotariu O, Ogden ID, Miller G, Dunn GM, Sheppard SK, Dallas JF, Reid TM, Howie H, Maiden MC, Forbes KJ. 2009. Attribution of Campylobacter infections in northeast Scotland to specific sources by use of multilocus sequence typing. J Infect Dis 199: 1205-1208. http://dx.doi.org/10.1086/597417.
8. Szewzyk U, Szewzyk R, Manz W, Schleiffer KH. 2000. Microbiological safety of drinking water. Annu Rev Microbiol 54:81-127. http://dx.doi.org/10.1146/annurev.micro.54.1.81.
9. Sheppard SK, Colles FM, McCarthy ND, Strachan NJ, Ogden ID, Forbes KJ, Dallas JF, Maiden MC. 2011. Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Mol Ecol 20:3484-3490. http://dx.doi.org/10.1111/j.1365-294X.2011.05179.x.
10. Manning G, Dowson CG, Bagnall MC, Ahmed IH, West M, Newell DG. 2003. Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni. Appl Environ Microbiol 69:6370-6379. http://dx.doi.org/10.1128/AEM.69.11.6370-6379.2003.
11. Milnes AS, Stewart I, Clifton-Hadley FA, Davies RH, Newell DG, Sayers AR, Cheasty T, Cassar C, Ridley A, Cook AJC, Evans SJ, Teale CJ, Smith RP, McNally A, Toszeghy M, Futter R, Kay A, Paiba GA. 2008. Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol Infect 136:739-751. http://dx.doi.org/10.1017/S0950268807009223.
12. Sheppard SK, Dallas JF, Strachan NJ, MacRae M, McCarthy ND, Wilson DJ, Gormley FJ, Falush D, Ogden ID, Maiden MC, Forbes KJ. 2009. Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 48:1072-1078. http://dx.doi.org/10.1086/597402.
13. Wilson DJ, Gabriel E, Leatherbarrow AJ, Cheesbrough J, Gee S, Bolton E, Fox A, Fearnhead P, Hart CA, Diggle PJ. 2008. Tracing the source of campylobacteriosis. PLoS Genet 4:e1000203. http://dx.doi.org/10.1371/journal.pgen.1000203.
14. Sheppard SK, Didelot X, Meric G, Torralbo A, Jolley KA, Kelly DJ, Bentley SD, Maiden MC, Parkhill J, Falush D. 2013. Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc Natl Acad Sci U S A 110:11923-11927. http://dx.doi.org/10.1073/pnas.1305559110.
15. Tang J, Hanage WP, Fraser C, Corander J. 2009. Identifying currents in the gene pool for bacterial populations using an integrative approach. PLoS Comput Biol 5:e1000455. http://dx.doi.org/10.1371/journal.pcbi .1000455.
16. Feil EJ, Maynard Smith J, Enright MC, Spratt BG. 2000. Estimating the recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154:1439-1450.
17. Fearnhead P, Smith NG, Barrigas M, Fox A, French N. 2005. Analysis of recombination in Campylobacter jejuni from MLST population data. J Mol Evol 61:333-340. http://dx.doi.org/10.1007/s00239-004-0316-0.
18. Wilson DJ, Gabriel E, Leatherbarrow AJ, Cheesbrough J, Gee S, Bolton E, Fox A, Hart CA, Diggle PJ, Fearnhead P. 2009. Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol 26:385-397. http://dx.doi.org/10.1093/molbev/msn264.
19. Sheppard SK, McCarthy ND, Falush D, Maiden MC. 2008. Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237-239. http://dx.doi.org/10.1126/science.1155532.
20. Zerbino D, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi .org/10.1101/gr.074492.107.
21. Swain MT, Tsai IJ, Assefa SA, Newbold C, Berriman M, Otto TD. 2012. A post-assembly genome-improvement toolkit (PAGIT) to obtain annotated genomes from contigs. Nat Protoc 7:1260-1284. http://dx.doi.org/10.1038/nprot.2012.068.
22. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068-2069. http://dx.doi.org/10.1093/bioinformatics/btu153.
23. Katoh K, Standley D. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772-780. http://dx.doi.org/10.1093/molbev/mst010.
24. Jolley KS, Maiden MC. 2010. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595. http://dx.doi.org/10.1186/1471-2105-11-595.
25. Price M, Dehal PAA. 2010. FastTree2-approximately maximumlikelihood trees for large alignments. PLoS One 5:e9490. http://dx.doi.org/10.1371/journal.pone.0009490.
26. Blom J, Albaum S, Doppmeier D, Puhler A, Vorholter F, Zakrzewski M, Goesmann A. 2009. EDGAR: a software for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10:154. http://dx.doi.org/10.1186/1471-2105-10-154.
27. Marttinen P, Hanage WP, Croucher NJ, Connor TR, Harris SR, Bentley SD, Corander J. 2012. Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res 40:e6. http://dx.doi.org/10.1093/nar/gkr928.
28. Duim B, Godschalk PC, van den Braak N, Dingle KE, Dijkstra JR, Leyde E, van der Plas J, Colles FM, Endtz HP, Wagenaar JA, Maiden MC, van Belkum A. 2003. Molecular evidence for dissemination of unique Campylobacter jejuni clones in Curacao, Netherlands Antilles. J Clin Microbiol 41:5593-5597. http://dx.doi.org/10.1128/JCM.41.12.5593-5597.2003.
29. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, Bootsma HJ, Willems RJ, Urwin R, Maiden MC. 2001. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39:14-23. http://dx.doi .org/10.1128/JCM.39.1.14-23.2001.
30. Ahmed IH, Manning G, Wassenaar TM, Cawthraw S, Newell DG. 2002. Identification of genetic differences between two Campylobacter jejuni strains with different colonization potentials. Microbiology 148:1203-1212.
31. Poly F, Threadgill D, Stintzi A. 2004. Identification of Campylobacter jejuni ATCC 43431-specific genes by whole microbial genome comparisons. J Bacteriol 186:4781-4795. http://dx.doi.org/10.1128/JB.186.14.4781-4795.2004.
32. Poly F, Threadgill D, Stintzi A. 2005. Genomic diversity in Campylobacter jejuni: identification of C. jejuni 81-176-specific genes. J Clin Microbiol 43:2330-2338. http://dx.doi.org/10.1128/JCM.43.5.2330-2338.2005.
33. Holt J, Grant A, Coward C, Maskell DQJ. 2012. Identification of Cj1051c as a major determinant for the restriction barrier of Campylobacter jejuni strain NCTC11168. Appl Environ Microbiol 78:7841-7848. http://dx.doi .org/10.1128/AEM.01799-12.
34. Asakura H, Bruggemann H, Sheppard S, Ekawa T, Meyer T, Yamamoto SIS. 2012. Molecular evidence for the thriving of Campylobacter jejuni ST4256 in Japan. PLoS One 7:e48394. http://dx.doi.org/10.1371/journal .pone.0048394.
35. Budroni S, Siena E, Dunning-Hotopp J, Seib K, Serruto D, Nofroni C, Comanducci M, Riley D, Daughery S, Angiuoli S, Covacci A, Pizza M, Rappuoli R, Moxon ER, Tettelin HMD. 2011. Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proc Natl Acad Sci U S A 108: 4494-4499. http://dx.doi.org/10.1073/pnas.1019751108.
36. McCarthy ND, Colles FM, Dingle KE, Bagnall MC, Manning G, Maiden MC, Falush D. 2007. Host-associated genetic import in Campylobacter jejuni. Emerg Infect Dis 13:267-272. http://dx.doi.org/10.3201/eid1302.060620.
37. Reuter S, Connor TR, Barquist L, Walker D, Feltwell T, Harris SR, Fookes M, Hall ME, Petty NK, Fuchs TM, Corander J, Dufour M, Ringwood T, Savin C, Bouchier C, Martin L, Miettinen M, Shubin M, Riehm JM, Laukkanen-Ninios R, Sihvonen LM, Siitonen A, Skurnik M, Falcão JP, Fukushima H, Scholz HC, Prentice MB, Wren BW, Parkhill J, Carniel E, Achtman M, McNally A, Thomson NR. 2014. Parallel independent evolution of pathogenicity within the genus Yersinia. Proc Natl Acad Sci U S A 111:6768-6773. http://dx.doi.org/10.1073/pnas .1317161111.
38. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O'Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852. http://dx.doi.org/10.1038/35101607.
39. Zeng X, Xu F, Mo YLJ. 2013. Identification and characterisation of a periplasmic trilactone esterase, Cee, revealed unique features of ferric enterobactin acquistion in Campylobacter. Mol Microbiol 87:594-608. http://dx.doi.org/10.1111/mmi.12118.