Comparative genomic analyses reveal diverse virulence factors and antimicrobial resistance mechanisms in clinical Elizabethkingia meningoseptica strains


Autoři: Shicheng Chen aff001;  Marty Soehnlen aff002;  Jochen Blom aff003;  Nicolas Terrapon aff004;  Bernard Henrissat aff004;  Edward D. Walker aff001
Působiště autorů: Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United States of America aff001;  Michigan Department of Health and Human Services, Bureau of Laboratories, Lansing, MI, United States of America aff002;  Bioinformatics and Systems Biology, Justus-Liebig-University, Giessen, Germany aff003;  Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille Université (AMU), UMR 7257, Marseille, France aff004;  Institut National de la Recherche Agronomique (INRA), USC 1408 AFMB, Marseille, France aff005;  Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia aff006
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222648

Souhrn

Three human clinical isolates of bacteria (designated strains Em1, Em2 and Em3) had high average nucleotide identity (ANI) to Elizabethkingia meningoseptica. Their genome sizes (3.89, 4.04 and 4.04 Mb) were comparable to those of other Elizabethkingia species and strains, and exhibited open pan-genome characteristics, with two strains being nearly identical and the third divergent. These strains were susceptible only to trimethoprim/sulfamethoxazole and ciprofloxacin amongst 16 antibiotics in minimum inhibitory tests. The resistome exhibited a high diversity of resistance genes, including 5 different lactamase- and 18 efflux protein- encoding genes. Forty-four genes encoding virulence factors were conserved among the strains. Sialic acid transporters and curli synthesis genes were well conserved in E. meningoseptica but absent in E. anophelis and E. miricola. E. meningoseptica carried several genes contributing to biofilm formation. 58 glycoside hydrolases (GH) and 25 putative polysaccharide utilization loci (PULs) were found. The strains carried numerous genes encoding two-component system proteins (56), transcription factor proteins (187~191), and DNA-binding proteins (6~7). Several prophages and CRISPR/Cas elements were uniquely present in the genomes.

Klíčová slova:

Antibiotic resistance – Antibiotics – Antimicrobial resistance – Comparative genomics – DNA-binding proteins – Genome analysis – Sialic acids – Virulence factors


Zdroje

1. Jacobs A, Chenia HY. Biofilm formation and adherence characteristics of an Elizabethkingia meningoseptica isolate from Oreochromis mossambicus. Ann Clin Microbiol Antimicrob. 2011;10:16–. doi: 10.1186/1476-0711-10-16 PMC3112384. 21545730

2. Luke SPM, Daniel SO, Annette J, Jane FT, Simon A, Hugo D, et al. Waterborne Elizabethkingia meningoseptica in adult critical care. Emerg Infect Diseases. 2016;22(1):9. doi: 10.3201/eid2201.150139 26690562

3. Hsu M-S, Liao C-H, Huang Y-T, Liu C-Y, Yang C-J, Kao K-L, et al. Clinical features, antimicrobial susceptibilities, and outcomes of Elizabethkingia meningoseptica (Chryseobacterium meningosepticum) bacteremia at a medical center in Taiwan, 1999–2006. Eur J Clin Microbiol Infect Dis 2011;30(10):1271–8. doi: 10.1007/s10096-011-1223-0 21461847

4. Jean SS, Lee WS, Chen FL, Ou TY, Hsueh PR. Elizabethkingia meningoseptica: an important emerging pathogen causing healthcare-associated infections. J Hosp Infect. 2014;86(4):244–9. doi: 10.1016/j.jhin.2014.01.009 24680187

5. Balm MND, Salmon S, Jureen R, Teo C, Mahdi R, Seetoh T, et al. Bad design, bad practices, bad bugs: frustrations in controlling an outbreak of Elizabethkingia meningoseptica in intensive care units. J Hosp Infect 2013;85(2):134–40. doi: 10.1016/j.jhin.2013.05.012 23958153

6. Chawla K, Gopinathan A, Varma M, Mukhopadhyay C. Elizabethkingia meningoseptica outbreak in intensive care unit. J Global Infect Dis. 2015;7(1):43–4. doi: 10.4103/0974-777X.150890 25722622.

7. Chang Y-C, Lo H-H, Hsieh H-Y, Chang S-M. Identification and epidemiological relatedness of clinical Elizabethkingia meningoseptica isolates from central Taiwan. J Microbiol Immunol Infect 2014;47(4):318–23. doi: 10.1016/j.jmii.2013.03.007 23726463

8. de Carvalho Filho ÉB, Marson FAL, Levy CE. Challenges in the identification of Chryseobacterium indologenes and Elizabethkingia meningoseptica in cases of nosocomial infections and patients with cystic fibrosis. New Microbes New Infect. 2017;20:27–33. doi: 10.1016/j.nmni.2017.09.002 29062487.

9. Cenk MH, Özlem T, Serpil Ö, Burçin Ş, Dilşa TG, Uğur Ö, et al. Clinical strains of Chryseobacterium and Elizabethkingia spp. isolated from pediatric patients in a university hospital: performance of MALDI-TOF MS-based identification, antimicrobial susceptibilities, and baseline patient characteristics. Microbial Drug Resistance. 2018;24(6):816–21. doi: 10.1089/mdr.2017.0206 29227188.

10. Lau SKP, Chow W-N, Foo C-H, Curreem SOT, Lo GC-S, Teng JLL, et al. Elizabethkingia anophelis bacteremia is associated with clinically significant infections and high mortality. Sci Rep. 2016;6:26045. doi: 10.1038/srep26045 PMC4868968. 27185741

11. Kim KK, Kim MK, Lim JH, Park HY, Lee S-T. Transfer of Chryseobacterium meningosepticum and Chryseobacterium miricola to Elizabethkingia gen. nov. as Elizabethkingia meningoseptica comb. nov. and Elizabethkingia miricola comb. nov. Int J Syst Evol Microbiol. 2005;55(3):1287–93. doi: 10.1099/ijs.0.63541–0

12. Chew KL, Cheng B, Lin RTP, Teo JWP. Elizabethkingia anophelis is the dominant Elizabethkingia species found in blood cultures in Singapore. J Clin Microbiol. 2018;56(3):e01445–17. doi: 10.1128/JCM.01445-17 29237782.

13. Han M-S, Kim H, Lee Y, Kim M, Ku NS, Choi JY, et al. Relative prevalence and antimicrobial susceptibility of clinical isolates of Elizabethkingia species based on 16S rRNA gene sequencing. J Clin Microbiol. 2017;55(1):274–80. doi: 10.1128/JCM.01637-16 27847376

14. Opota O, Diene SM, Bertelli C, Prod'hom G, Eckert P, Greub G. Genome of the carbapenemase-producing clinical isolate Elizabethkingia miricola EM_CHUV and comparative genomics with Elizabethkingia meningoseptica and Elizabethkingia anophelis: evidence for intrinsic multidrug resistance trait of emerging pathogens. Int J Antimicrob Agents. 2017;49(1):93–7. doi: 10.1016/j.ijantimicag.2016.09.031 27913093

15. González LJ, Vila AJ. Carbapenem resistance in Elizabethkingia meningoseptica is mediated by metallo-β-lactamase BlaB. Antimicrob Agents and Chemother. 2012;56(4):1686–92. doi: 10.1128/aac.05835-11 22290979

16. Perrin A, Larsonneur E, Nicholson AC, Edwards DJ, Gundlach KM, Whitney AM, et al. Evolutionary dynamics and genomic features of the Elizabethkingia anophelis 2015 to 2016 Wisconsin outbreak strain. Nat Commun. 2017;8:15483. doi: 10.1038/ncomms15483 https://www.nature.com/articles/ncomms15483-supplementary-information. 28537263

17. Lin J-N, Lai C-H, Yang C-H, Huang Y-H, Lin H-H. Genomic features, phylogenetic relationships, and comparative genomics of Elizabethkingia anophelis strain EM361-97 isolated in Taiwan. Sci Rep. 2017;7(1):14317. doi: 10.1038/s41598-017-14841-8 29085032

18. Michael Janda J., Lopez DL. Mini review: New pathogen profiles: Elizabethkingia anophelis. Diagn Microbiol Infect Dis 2017;88(2):201–5. doi: 10.1016/j.diagmicrobio.2017.03.007 28342565

19. CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 26th ed. CLSI supplement M100S. Wayne PCaLSI.

20. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77. doi: 10.1089/cmb.2012.0021 PMC3342519. 22506599

21. 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 Acids Res. 2014;42(Database issue):D206–D14. doi: 10.1093/nar/gkt1226 PMC3965101. 24293654

22. Montaner B, Navarro S, Piqué M, Vilaseca M, Martinell M, Giralt E, et al. Prodigiosin from the supernatant of Serratia marcescens induces apoptosis in haematopoietic cancer cell lines. Br J Pharmacol. 2000;131(3):585–93. doi: 10.1038/sj.bjp.0703614 PMC1572367. 11015311

23. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: A Fast Phage Search Tool. Nucleic Acids Research. 2011. doi: 10.1093/nar/gkr485 21672955

24. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35(suppl 2):W52–W7. doi: 10.1093/nar/gkm360 17537822

25. Blom J, Kreis J, Spänig S, Juhre T, Bertelli C, Ernst C, et al. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res. 2016:W22–W8. doi: 10.1093/nar/gkw255 27098043

26. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial “pan-genome”. PNAS USA. 2005;102(39):13950–5. doi: 10.1073/pnas.0506758102 16172379

27. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147

28. Felsenstein J. PHYLIP—phylogeny inference package (Version 3.2). Cladistics. 1989;5:164–6.

29. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42(D1):D490–D5. doi: 10.1093/nar/gkt1178 24270786

30. Chen S, Blom J, Walker ED. Genomic, physiologic, and symbiotic characterization of Serratia marcescens strains isolated from the mosquito Anopheles stephensi. Front Microbiol. 2017;8(1483). doi: 10.3389/fmicb.2017.01483 28861046

31. 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

32. Terrapon N, Lombard V, Drula É, Lapébie P, Al-Masaudi S, Gilbert HJ, et al. PULDB: the expanded database of polysaccharide utilization loci. Nucleic Acids Res. 2018;46(D1):D677–D83. doi: 10.1093/nar/gkx1022 29088389

33. Foley MH, Cockburn DW, Koropatkin NM. The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cellular and molecular life sciences: CMLS. 2016;73(14):2603–17. doi: 10.1007/s00018-016-2242-x 27137179.

34. Duchaud E, Rochat T, Habib C, Barbier P, Loux V, Guérin C, et al. Genomic Diversity and Evolution of the Fish Pathogen Flavobacterium psychrophilum. Frontiers in Microbiology. 2018;9(138). doi: 10.3389/fmicb.2018.00138 29467746

35. Chen S, Blom J, Loch TP, Faisal M, Walker ED. The emerging fish pathogen Flavobacterium spartansii isolated from chinook salmon: comparative genome analysis and molecular manipulation. Front Microbiol. 2017;8(2339). doi: 10.3389/fmicb.2017.02339 29250046

36. Teo J, Tan SY-Y, Liu Y, Tay M, Ding Y, Li Y, et al. Comparative genomic analysis of malaria mosquito vector associated novel pathogen Elizabethkingia anophelis. Genome Biol Evol 2014: doi: 10.1093/gbe/evu094 24803570

37. Chen S, Zhao J, Joshi D, Xi Z, Norman B, Walker ED. Persistent infection by Wolbachia wAlbB has no effect on composition of the gut microbiota in adult female Anopheles stephensi. Front Microbiol. 2016;7(1485). doi: 10.3389/fmicb.2016.01485 27708633

38. Akhouayri IG, Habtewold T, Christophides GK. Melanotic pathology and vertical transmission of the gut commensal Elizabethkingia meningoseptica in the major malaria vector Anopheles gambiae. PLoS ONE. 2013;8(10):e77619. doi: 10.1371/journal.pone.0077619 24098592

39. Dodd D, Moon YH, Swaminathan K, Mackie RI, Cann IK. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. J Biol Chem. 2010;285(39):30261–73. Epub 2010/07/14. doi: 10.1074/jbc.M110.141788 20622018; PubMed Central PMCID: PMC2943253.

40. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289–306. doi: 10.4161/gmic.19897 PMC3463488. 22572875

41. Kolton M, Sela N, Elad Y, Cytryn E. Comparative genomic analysis indicates that niche adaptation of terrestrial Flavobacteria is strongly linked to plant glycan metabolism. PLoS ONE. 2013;8(9):e76704. doi: 10.1371/journal.pone.0076704 PMC3784431. 24086761

42. Chen S, Kaufman MG, Miazgowicz KL, Bagdasarian M, Walker ED. Molecular characterization of a cold-active recombinant xylanase from Flavobacterium johnsoniae and its applicability in xylan hydrolysis. Bioresour Technol. 2013;128(0):145–55. http://dx.doi.org/10.1016/j.biortech.2012.10.087.

43. Nagal S, Jain PC. Production of feather hydrolysate by Elizabethkingia meningoseptica KB042 (MTCC 8360) in submerged fermentation. ndian J Microbiol. 2010;50(1):41–5. doi: 10.1007/s12088-010-0014-0 22815570

44. Tekedar HC, Karsi A, Reddy JS, Nho SW, Kalindamar S, Lawrence ML. Comparative genomics and transcriptional analysis of Flavobacterium columnare strain ATCC 49512. Front Microbiol. 2017;8(588). doi: 10.3389/fmicb.2017.00588 28469601

45. Yoshizawa S, Kumagai Y, Kim H, Ogura Y, Hayashi T, Iwasaki W, et al. Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria. Proc Natl Acad Sci U S A 2014;111(18):6732–7. doi: 10.1073/pnas.1403051111 24706784

46. Kukutla P, Lindberg BG, Pei D, Rayl M, Yu W, Steritz M, et al. Insights from the genome annotation of Elizabethkingia anophelis from the malaria vector Anopheles gambiae. PLoS ONE. 2014;9(5):10.1371/journal.pone.0097715. doi: 10.1371/journal.pone.0097715 24842809

47. Kämpfer P, Busse H-J, McInroy JA, Glaeser SP. Elizabethkingia endophytica sp. nov., isolated from Zea mays and emended description of Elizabethkingia anophelis Kämpfer et al. 2011. Int J Syst Evol Microbiol. 2015;65(7):2187–93. doi: 10.1099/ijs.0.000236 25858248

48. Kämpfer P, Matthews H, Glaeser SP, Martin K, Lodders N, Faye I. Elizabethkingia anophelis sp. nov., isolated from the midgut of the mosquito Anopheles gambiae. Int J Syst Evol Microbiol. 2011;61(11):2670–5. doi: 10.1099/ijs.0.026393–0

49. Chen S, Bagdasarian M, Walker ED. Elizabethkingia anophelis: molecular manipulation and interactions with mosquito hosts. Appl Environ Microbiol. 2015. doi: 10.1128/aem.03733-14 25595771

50. Ruixue H, Junfa Y, Yin M, Zhe W, Zemao G. Pathogenic Elizabethkingia miricola infection in cultured black-spotted frogs, China, 2016. Emerg Infect Diseases. 2017;23(12):2055. doi: 10.3201/eid2312.170942 29148374

51. Chen S, Soehnlen M, Downes FP, Walker ED. Insights from the draft genome into the pathogenicity of a clinical isolate of Elizabethkingia meningoseptica Em3. Stand Genomic Sci. 2017;12:56. doi: 10.1186/s40793-017-0269-8 PMC5602931. 28932346

52. Darvish Alipour Astaneh S, Rasooli I, Mousavi Gargari SL. The role of filamentous hemagglutinin adhesin in adherence and biofilm formation in Acinetobacter baumannii ATCC19606(T). Microb Pathog. 2014;74:42–9. doi: 10.1016/j.micpath.2014.07.007 25086432.

53. Cioffi DL, Pandey S, Alvarez DF, Cioffi EA. Terminal sialic acids are an important determinant of pulmonary endothelial barrier integrity. Am J Physiol Lung Cell Mol Physiol. 2012;302(10):L1067–L77. doi: 10.1152/ajplung.00190.2011 PMC3362258. 22387293

54. Reutter W, Stäsche R, Stehling P, Baum O. The biology of sialic acids: insights into their structure, metabolism and function in particular during viral infection. Glycosciences.

55. Opal SM. Significance of sialic acid in Klebsiella pneumoniae K1 capsules. Virulence. 2014;5(6):648–9. doi: 10.4161/viru.34349 PMC4139404. 25105481

56. Anderson GG, Goller CC, Justice S, Hultgren SJ, Seed PC. Polysaccharide capsule and sialic acid-mediated regulation promote biofilm-like intracellular bacterial communities during cystitis. Infect Immun. 2010;78(3):963–75. doi: 10.1128/IAI.00925-09 20086090

57. McDonald ND, Lubin J-B, Chowdhury N, Boyd EF. Host-derived sialic acids are an important nutrient source required for optimal bacterial fitness in vivo. mBio. 2016;7(2). doi: 10.1128/mBio.02237-15 27073099

58. Severi E, Hood DW, Thomas GH. Sialic acid utilization by bacterial pathogens. Microbiol. 2007;153(9):2817–22. doi: 10.1099/mic.0.2007/009480-0 17768226

59. Hardy L, Jespers V, Van den Bulck M, Buyze J, Mwambarangwe L, Musengamana V, et al. The presence of the putative Gardnerella vaginalis sialidase A gene in vaginal specimens is associated with bacterial vaginosis biofilm. PLOS ONE. 2017;12(2):e0172522. doi: 10.1371/journal.pone.0172522 28241058

60. Honma K, Mishima E, Sharma A. Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect Immun. 2011;79(1):393–401. doi: 10.1128/IAI.00629-10 21078857

61. Leclercq R, Cantón R, Brown DFJ, Giske CG, Heisig P, MacGowan AP, et al. EUCAST expert rules in antimicrobial susceptibility testing. Clin Microbiol Infect. 2013;19(2):141–60. doi: 10.1111/j.1469-0691.2011.03703.x 22117544

62. Munita JM, Arias CA. Mechanisms of antibiotic resistance. Microbiol Spectr. 2016;4(2):10.1128/microbiolspec.VMBF-0016-2015. doi: 10.1128/microbiolspec.VMBF-0016-2015 PMC4888801. 27227291

63. Thabit AK, Crandon JL, Nicolau DP. Antimicrobial resistance: impact on clinical and economic outcomes and the need for new antimicrobials. Expert Opin Pharmacother. 2015;16(2):159–77. doi: 10.1517/14656566.2015.993381 25496207

64. Lin J-N, Lai C-H, Yang C-H, Huang Y-H, Lin H-H. Genomic features, phylogenetic relationships, and comparative genomics of Elizabethkingia anophelis strain EM361-97 isolated in Taiwan. Scientific Reports. 2017;7(1):14317. doi: 10.1038/s41598-017-14841-8 29085032

65. Li X-Z, Plésiat P, Nikaido H. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin Microbiol Rev 2015;28(2):337–418. doi: 10.1128/CMR.00117-14 25788514

66. Burns JL, Hedin LA, Lien DM. Chloramphenicol resistance in Pseudomonas cepacia because of decreased permeability. Antimicrob Agents Chemother. 1989;33(2):136–41. doi: 10.1128/aac.33.2.136 2719457

67. Leclercq R. Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clin Infect Dis. 2002;34(4):482–92. doi: 10.1086/324626 11797175

68. Casas V, Miyake J, Balsley H, Roark J, Telles S, Leeds S, et al. Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California. FEMS Microbiol Lett. 2006;261(1):141–9. doi: 10.1111/j.1574-6968.2006.00345.x 16842371

69. Wagner PL, Waldor MK. Bacteriophage control of bacterial virulence. Infect Immun. 2002;70(8):3985–93. doi: 10.1128/IAI.70.8.3985-3993.2002 PMC128183. 12117903

70. Waldor MK, Friedman DI. Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol. 2005;8(4):459–65. doi: 10.1016/j.mib.2005.06.001 15979389

71. Dupuis M-È, Villion M, Magadán AH, Moineau S. CRISPR-Cas and restriction–modification systems are compatible and increase phage resistance. Nat Commun. 2013;4:2087. doi: 10.1038/ncomms3087 23820428


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