Campylobacter portucalensis sp. nov., a new species of Campylobacter isolated from the preputial mucosa of bulls


Autoři: Marta Filipa Silva aff001;  Gonçalo Pereira aff001;  Carla Carneiro aff001;  Andrew Hemphill aff002;  Luísa Mateus aff001;  Luís Lopes-da-Costa aff001;  Elisabete Silva aff001
Působiště autorů: CIISA - Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Lisboa, Portugal aff001;  Institute of Parasitology, Vetsuisse Faculty, University of Bern, Berne, Switzerland aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227500

Souhrn

A new species of the Campylobacter genus is described, isolated from the preputial mucosa of bulls (Bos taurus). The five isolates obtained exhibit characteristics of Campylobacter, being Gram-negative non-motile straight rods, oxidase positive, catalase negative and microaerophilic. Phenotypic characteristics and nucleotide sequence analysis of 16S rRNA and hsp60 genes demonstrated that these isolates belong to a novel species within the genus Campylobacter. Based on hsp60 gene phylogenetic analysis, the most related species are C. ureolyticus, C. blaseri and C. corcagiensis. The whole genome sequence analysis of isolate FMV-PI01 revealed that the average nucleotide identity with other Campylobacter species was less than 75%, which is far below the cut-off for isolates of the same species. However, whole genome sequence analysis identified coding sequences highly homologous with other Campylobacter spp. These included several virulence factor coding genes related with host cell adhesion and invasion, transporters involved in resistance to antimicrobials, and a type IV secretion system (T4SS), containing virB2-virB11/virD4 genes, highly homologous to the C. fetus subsp. venerealis. The genomic G+C content of isolate FMV-PI01 was 28.3%, which is one of the lowest values reported for species of the genus Campylobacter. For this species the name Campylobacter portucalensis sp. nov. is proposed, with FMV-PI01 (= LMG 31504, = CCUG 73856) as the type strain.

Klíčová slova:

Blood – Campylobacter – Invasive species – Phylogenetic analysis – Ribosomal RNA – Sequence analysis – Sequence databases – Cardiobacterium hominis


Zdroje

1. Vandamme P, Dewhirst FE, Paster BJ, On SLW. Genus I Campylobacter. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology. New York: Springer-Verlag: 2005 p. 1147–1160.

2. Gölz G, Rosner B, Hofreuter D, Josenhans C, Kreienbrock L, Löwenstein A, et al. Relevance of Campylobacter to public health—the need for a one health approach. Int J Med Microbiol. 2014;304(7):817–823. doi: 10.1016/j.ijmm.2014.08.015 25266744.

3. Sahin O, Yaeger M, Wu Z, Zhang Q. Campylobacter-associated diseases in animals. Annu Rev Anim Biosci. 2017;8(5):21–42. doi: 10.1146/annurev-animal-022516-022826 27860495.

4. Lastovica AJ, On SLW, Zhang L. The Family Campylobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes. Heidelberg: Springer; 2014. p. 307–335.

5. bacterio.net [Internet]. List of prokariotic names with standing in nomenclature (LPSN) [cited 2019 Jun 5]. Available from: http://www.bacterio.net/campylobacter.html

6. Shinha T. Fatal bacteremia caused by Campylobacter gracilis, United States. Emerg Infect Dis. 2015;21(6):1084–1085. doi: 10.3201/eid2106.142043 25988682.

7. Lawson AJ, On SLW, Logan JM, Stanley J. Campylobacter hominis sp. nov., from the human gastrointestinal tract. Int J Syst Evol Microbiol. 2001;51:651–660. doi: 10.1099/00207713-51-2-651 11321111.

8. Vandamme P, Debruyne L, De Brandt E, Falsen E. Reclassification of Bacteroides ureolyticus as Campylobacter ureolyticus comb. nov., and emended description of the genus Campylobacter. Int J Syst Evol Microbiol. 2010;60: 2016–2022. doi: 10.1099/ijs.0.017152-0 19801389.

9. Gilbert MJ, Zomer AL, Timmerman AJ, Spaninks MP, Rubio-García A, Rossen JW, et al. Campylobacter blaseri sp. nov., isolated from common seals (Phoca vitulina). Int J Syst Evol Microbiol. 2018;68(5):1787–1794. doi: 10.1099/ijsem.0.002742 29624164.

10. Hakkinen M, Heiska H, Hänninen ML. Prevalence of Campylobacter spp. in cattle in Finland and antimicrobial susceptibilities of bovine Campylobacter jejuni strains. Appl Environ Microbiol. 2007;73(10):3232–3238. doi: 10.1128/AEM.02579-06 17369335.

11. Inglis GD, Kalischuk LD, Busz HW, Kastelic JP. Colonization of cattle intestines by Campylobacter jejuni and Campylobacter lanienae. Appl Environ Microbiol. 2005;71(9):5145–5153. doi: 10.1128/AEM.71.9.5145-5153.2005 16151098.

12. Koziel M, Lucey B, Bullman S, Corcoran GD, Sleator RD. Molecular-based detection of the gastrointestinal pathogen Campylobacter ureolyticus in unpasteurized milk samples from two cattle farms in Ireland. Gut Pathog. 2012;4:14. doi: 10.1186/1757-4749-4-14 23151337.

13. Quinn PJ, Markey BK, Leonard FC, FitzPatrick ES, Fanning S, Hartigan PJ editors. Veterinary Microbiology and Microbial Disease. 2nd ed. Chichester: Wiley-Blackwell; 2011.

14. Michi NA, Favetto PH, Kastelic J, Cobo ER. A review of sexually transmitted bovine trichomoniasis and campylobacteriosis affecting cattle reproductive health. Theriogenology. 2016;85(5):781–791. doi: 10.1016/j.theriogenology.2015.10.037 26679515.

15. Monke HJ, Love BC, Wittum TE, Monke DR, Byrum BA. Effect of transport enrichment medium, transport time, and growth medium on the detection of Campylobacter fetus subsp. venerealis. J Vet Diagn Invest. 2002:14(1):35–39. doi: 10.1177/104063870201400107 12680641.

16. Chaban B, Guerra AG, Hendrick SH, Waldner CL, Hill JE. Isolation rates of Campylobacter fetus subsp. venerealis from bovine preputial samples via passive filtration on nonselective medium versus selective medium, with and without transport medium. Am J Vet Res. 2013;74(8):1066–1069. doi: 10.2460/ajvr.74.8.1066 23879843.

17. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012;13:134. doi: 10.1186/1471-2105-13-134 22708584.

18. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096 29722887.

19. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680. doi: 10.1093/nar/22.22.4673 7984417.

20. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991; 173 (2):697–703. doi: 10.1128/jb.173.2.697-703.1991 1987160.

21. Gorkiewicz G, Feierl G, Schober C, Dieber F, Köfer J, Zechner R, et al. Species-specific identification of campylobacters by partial 16S rRNA gene sequencing. J Clin Microbiol. 2003; 41(6):2537–2546. doi: 10.1128/JCM.41.6.2537-2546.2003 12791878.

22. On SLW, Holmes B. Effect of inoculum size on the phenotypic characterization of Campylobacter species. J Clin Microbiol. 1991;29(5):923–926 2056060.

23. On SLW, Holmes B. Reproducibility of tolerance tests that are useful in the identification of campylobacteria. J Clin Microbiol. 1991;29:1785– 1788 1774297

24. Public Health England [Internet]. UK standards for microbiology investigations: Motility test. [cited 2019 Nov 18]. Available from: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/762926/TP_21i4.pdf

25. Hemphill A, Croft SL. Electron microscopy in parasitology. In: Rogan MM, editor. Analytical parasitology. Heidelberg: Springer-Verlag: 1997 p. 227–268.

26. Hemphill A, Vonlaufen N, Naguleswaran A, Keller N, Riesen M, Guetg N, et al. Tissue culture and explant approaches to studying and visualizing Neospora caninum and its interactions with the host cell. Microsc Microanal. 2004;10(5):602–620. doi: 10.1017/S1431927604040930 15525434.

27. Basto AP, Müller J, Rubbiani R, Stibal D, Giannini F, Süss-Fink G, et al. Characterization of the activities of dinuclear thiolato-bridged arene ruthenium complexes against Toxoplasma gondii. Antimicrob Agents Chemother. 2017;24;61(9). doi: 10.1128/AAC.01031-17 28652238.

28. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75. doi: 10.1186/1471-2164-9-75 18261238.

29. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acid Res. 2014;42:206–214. doi: 10.1093/nar/gkt1226 24293654.

30. Richter M, Rosselló-Móra R, Glöckner FO, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics. 2016; 32(6):929–931. doi: 10.1093/bioinformatics/btv681 26576653.

31. Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J, Néron B, et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res, 46:246–251. doi: 10.1093/nar/gky425 29790974.

32. Cosentino S, Voldby Larsen M, Møller Aarestrup F, Lund O. PathogenFinder—Distinguishing friend from foe using bacterial whole genome sequence data. PLoS One. 2013;8(10):e77302. doi: 10.1371/journal.pone.0077302 24204795.

33. On SLW, Miller WG, Houf K, Fox JG, Vandamme P. Minimal standards for describing new species belonging to the families Campylobacteraceae and Helicobacteraceae: Campylobacter, Arcobacter, Helicobacter and Wolinella spp. Int J Syst Evol Microbiol. 2017;67:5296–5311. doi: 10.1099/ijsem.0.002255 29034857.

34. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Reviews. 2015;28(3):687–720. doi: 10.1128/CMR.00006-15 26062576.

35. Koziel M, O’Doherty P, Vandamme P, Corcoran GD, Sleator RD, Lucey B. Campylobacter corcagiensis sp. nov., isolated from faeces of captive lion-tailed macaques (Macaca silenus). Int J Syst Evol Microbiol. 2014;64:2878–2883. doi: 10.1099/ijs.0.063867-0 24876239.

36. Gilbert MJ, Miller WG, Leger JS, Chapman MH, Timmerman AJ, Duim B, et al. Campylobacter pinnipediorum sp. nov. isolated from pinnipeds, comprising Campylobacter pinnipediorum subsp. pinnipediorum subsp. nov. and Campylobacter pinnipediorum subsp. caledonicus susbp. nov. Int J Syst Evol Microbiol. 2017;67:1961–1968. doi: 10.1099/ijsem.0.001894 28629508.

37. Logan JM, Burnens A, Linton D, Lawson AJ, Stanley J. Campylobacter lanienae sp. nov., a new species isolated from workers in an abattoir. Int J Syst Evol Microbiol. 2000;50:865–872. doi: 10.1099/00207713-50-2-865 10758898.

38. Van TT, Elshagmani E, Gor MC, Scott PC, Moore RJ. Campylobacter hepaticus sp. nov., isolated from chickens with spotty liver disease. Int J Syst Evol Microbiol. 2016;66:4518–4524. doi: 10.1099/ijsem.0.001383 27498969.

39. Rossi M, Debruyne L, Zanoni RG, Manfreda G, Revez J, Vandamme P. Campylobacter avium sp. nov., a hippurate-positive species isolated from poultry. Int J Syst Evol Microbiol. 2009; 59:2364–2369. doi: 10.1099/ijs.0.007419-0 19620353.

40. Inglis GD, Hoar BM, Whiteside DP, Morck DW. Campylobacter canadensis sp. nov., from captive whooping cranes in Canada. Int J Syst Evol Microbiol. 2007;57:2636–2644. doi: 10.1099/ijs.0.65061-0 17978232.

41. Zanoni RG, Debruyne L, Rossi M, Revez J, Vandamme P. Campylobacter cuniculorum sp. nov., from rabbits. Int J Syst Evol Microbiol. 2009;59:1666–1671. doi: 10.1099/ijs.0.007286-0 19542108.

42. Piccirillo A, Niero G, Calleros L, Pérez R, Naya H, Iraola G. Campylobacter geochelonis sp. nov. isolated from the western hermann’s tortoise (Testudo hermanni hermanni). Int J Syst Evol Microbiol. 2016;66:3468–3476. doi: 10.1099/ijsem.0.001219 27266587.

43. Foster G, Holmes B, Steigerwalt AG, Lawson PA, Thorne P, Byrer DE, et al. Campylobacter insulaenigrae sp. nov., isolated from marine mammals. Int J Syst Evol Microbiol. 2004;54:2369–2373. doi: 10.1099/ijs.0.63147-0 15545485.

44. Debruyne L, Broman T, Bergström S, Olsen B, On SL, Vandamme P. Campylobacter subantarcticus sp. nov., isolated from birds in the sub-Antarctic region. Int J Syst Evol Microbiol. 2010;60:815–819. doi: 10.1099/ijs.0.011056-0 19661523.

45. Debruyne L, Broman T, Bergström S, Olsen B, On SL, Vandamme P. Campylobacter volucris sp. nov., isolated from black-headed gulls (Larus ridibundus). Int J Syst Evol Microbiol. 2010;60:1870–1875. doi: 10.1099/ijs.0.013748-0 19767353.

46. Gilbert MJ, Kik M, Miller WG, Duim B, Wagenaar JA. Campylobacter iguaniorum sp. nov., isolated from reptiles. Int J Syst Evol Microbiol. 2015;65:975–982. doi: 10.1099/ijs.0.000048 25574036.

47. Cáceres A, Muñoz I, Iraola G, Díaz-Viraqué F, Collado L. Campylobacter ornithocola sp. nov., a novel member of the Campylobacter lari group isolated from wild bird faecal samples. Int J Syst Evol Microbiol. 2017;67;1643–1649. doi: 10.1099/ijsem.0.001822 28126040.

48. Stackebrandt E, Goebel BM. A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol. 1994;44:846–49.

49. Sakamoto M, Ohkuma M. Usefulness of the hsp60 gene for the identification and classification of Gram-negative anaerobic rods. J Med Microbiol. 2010;59:1293–1302. doi: 10.1099/jmm.0.020420-0 20671088.

50. Kärenlampi RI, Tolvanen TP, Hänninen ML. Phylogenetic analysis and PCR-restriction fragment length polymorphism identification of Campylobacter species based on partial groEL gene sequences. J Clin Microbiol. 2004; 42 (12): 5731–5738. doi: 10.1128/JCM.42.12.5731-5738.2004 15583306.

51. Rocha EP, Danchin A. Base composition bias might result from competition for metabolic resources. Trends Genet. 2002;18:291–294. doi: 10.1016/S0168-9525(02)02690-2 12044357.

52. Mann S, Chen YP. Bacterial genomic G+C composition-eliciting environmental adaptation. Genomics. 2010;95:7–15. doi: 10.1016/j.ygeno.2009.09.002 19747541.

53. Iraola G, Pérez R, Naya H, Paolicchi F, Pastor E, Valenzueça S, et al. Genomic evidence for emergence and evolution of pathogenicity and niche preferences in the genus Campylobacter. Genome Biol Evol. 2014;6(9):2392–2405. doi: 10.1093/gbe/evu195 25193310.

54. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;106(45):19126–19131. doi: 10.1073/pnas.0906412106 19855009.

55. Louwen R, Staals RHJ, Endtz HP, van Baarlen P, van der Oost J. The role of CRISPR-Cas systems in virulence of pathogenic bacteria. Microbiol Mol Biol Rev. 2014;78:74–88. doi: 10.1128/MMBR.00039-13 24600041.

56. Westra ER, van Houte S, Gandon S, Whitaker R. The ecology and evolution of microbial CRISPR-Cas adaptive immune systems. Philos Trans R Soc Lond B Biol Sci. 2019;374(1772):20190101. doi: 10.1098/rstb.2019.0101 30905294.

57. Ali A, Soares SC, Santos AR, Guimarães LC, Barbosa E, Almeida SS, et al. Campylobacter fetus subspecies: comparative genomics and prediction of potential virulence targets. Gene. 2012;508(2):145–56. doi: 10.1016/j.gene.2012.07.070 22890137.

58. Krause-Gruszczynska M, van Alphen LB, Oyarzabal OA, Alter T, Hänel I, Schliephake A, et al. Expression patterns and role of CadF protein in Campylobacter jejuni and Campylobacter coli. FEMS Microbiol Lett. 2007;274:9–16. doi: 10.1111/j.1574-6968.2007.00802.x 17573935.

59. Ziprin RL, Young CR, Stanker LH, Hume ME, Konkel ME. The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein. Avian Dis. 1999;43(3):686–589 10494431.

60. Monteville MR, Yoon JE, Konkel ME. Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology. 2003;149:153–165. doi: 10.1099/mic.0.25820-0 12576589.

61. Konkel ME, Kim BJ, Rivera-Amill V, Garvis SG. Identification of proteins required for the internalization of Campylobacter jejuni into cultured mammalian cells. Adv Exp Med Biol. 1999;473:215–224. doi: 10.1007/978-1-4615-4143-1_22 10659361.

62. Konkel ME, Kim BJ, Rivera-Amill V, Garvis SG. Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Mol Microbiol. 1999;32(4):691–701. doi: 10.1046/j.1365-2958.1999.01376.x 10361274.

63. Guo B, Lin J, Reynolds DL, Zhang Q. Contribution of the multidrug efflux transporter CmeABC to antibiotic resistance in different Campylobacter species. Foodborne Pathog Dis. 2010;7(1):77–83. doi: 10.1089/fpd.2009.0354 19785541.

64. Lin J, Sahin O, Michel LO, Zhang Q. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun. 2003;71(8):4250–4259. doi: 10.1128/IAI.71.8.4250-4259.2003 12874300.

65. Gibreel A, Wetsch NM, Taylor DE. Contribution of the CmeABC efflux pump to macrolide and tetracycline resistance in Campylobacter jejuni. Antimicrob Agents Chemother. 2007;51(9):3212–3216. doi: 10.1128/AAC.01592-06 17606685.

66. Lin J, Michel LO, Zhang Q. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob Agents Chemother. 2002;46(7):2124–2131. doi: 10.1128/AAC.46.7.2124-2131.2002 12069964.

67. Gorkiewicz G, Kienesberger S, Schober C, Scheicher SR, Gülly C, Zechner R, et al. A genomic island defines susbspecies-specific virulence features of the host-adapted pathogen Campylobacter fetus subsp. venerealis. J Bacteriol. 2010;192(2):502–517. doi: 10.1128/JB.00803-09 19897645.

68. Kienesberger S, Trummler CS, Fauster A, Lang S, Sprenger H, Gorkiewicz G, et al. Interbacterial macromolecular transfer by the Campylobacter fetus subsp. venerealis type IV secretion system. J Bacteriol. 2011;193(3):744–758. doi: 10.1128/JB.00798-10 21115658.


Článek vyšel v časopise

PLOS One


2020 Číslo 1