A pan-genomic approach to understand the basis of host adaptation in achromobacter

Genome Biology and Evolution

Volumn 9, Issue 4, 2017, Pages 1030-1046

  Jeukens, Julie ^a   Freschi, Luca ^a   Vincent, Antony T ^a,b   Emond Rheault, Jean Guillaume ^a   Kukavica Ibrulj, Irena ^a   Charette, Steve J ^a,b   Levesque, Roger C ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Antibiotic resistance; Comparative genomics; Horizontal gene transfer; Mobilome; Phylogenomics

Indexed keywords

EID: 85020656401     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evx061     Document Type: Article

References (88)

1. Abbott IJ, Peleg AY. 2015. Stenotrophomonas, Achromobacter, and nonmelioid Burkholderia species: antimicrobial resistance and therapeutic strategies. Semin Respir Crit Care Med. 36:99-110.
2. Abby SS, Rocha EPC. 2012. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. Plos Genet. 8:e1002983.
3. Alcalde-Rico M, Hernando-Amado S, Blanco P, Martínez JL. 2016. Multidrug efflux pumps at the crossroad between antibiotic resistance and bacterial virulence. Front Microbiol. 7:14.
4. Almuzara M, et al. 2010. In vitro susceptibility of Achromobacter spp. isolates: comparison of disk diffusion, Etest and agar dilution methods. Int J Antimicrob Agents 35:68-71.
5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
6. Amoureux L, et al. 2013a. Detection of Achromobacter xylosoxidans in hospital, domestic, and outdoor environmental samples and comparison with human clinical isolates. Appl Environ Microbiol. 79:7142- 7149.
7. Amoureux L, et al. 2013b. Epidemiology and resistance of Achromobacter xylosoxidans from cystic fibrosis patients in Dijon, Burgundy: first French data. J Cyst Fibros. 12:170-176.
8. Amoureux L, et al. 2016. Achromobacter xylosoxidans is the predominant Achromobacter species isolated from diverse non-respiratory samples. Epidemiol Infect. 18:1-4.
9. Bador J, Amoureux L, Blanc E, Neuwirth C. 2013. Innate aminoglycoside resistance of Achromobacter xylosoxidans is due to AxyXY-OprZ, an RND-type multidrug efflux pump. Antimicrob Agents Chemother. 57:603-605.
10. Bador J, et al. 2011. First description of an RND-type multidrug efflux pump in Achromobacter xylosoxidans, Axy ABM. Antimicrob Agents Chemother. 55:4912-4914.
11. Bador J, et al. 2016. Distribution of innate efflux-mediated aminoglycoside resistance among different Achromobacter species. N Microbes N Infect. 10:1-5.
12. Bradley P, et al. 2015. Rapid antibiotic-resistance predictions from genome sequence data for Staphylococcus aureus and Mycobacterium tuberculosis. Nat Commun. 6:15.
13. Coburn B, Sekirov I, Finlay BB. 2007. Type III secretion systems and disease. Clin Microbiol Rev. 20:535-549.
14. Cools P, et al. 2015. A single clone of Achromobacter xylosoxidans colonizes Belgian cystic fibrosis patients from different centres. J Cystic Fibros. 14(Suppl 1):S76.
15. Cools P, et al. 2016. Epidemic Achromobacter xylosoxidans strain among Belgian cystic fibrosis patients and review of literature. BMC Microbiol. 16:1-13.
16. Coward A, et al. 2016. Use of nrdA gene sequence clustering to estimate the prevalence of different Achromobacter species among cystic fibrosis patients in the UK. J Cystic Fibros. 15:479-485.
17. Criscuolo A, Gribaldo S. 2010. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 10:1-21.
18. Darriba D, Taboada GL, Doallo R, Posada D. 2012. JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772- 772.
19. Davies JC, Rubin BK. 2007. Emerging and unusual Gram-negative infections in cystic fibrosis. Semin Respir Crit Care Med. 28:312-321.
20. Doi Y, Poirel L, Paterson DL, Nordmann P. 2008. Characterization of a naturally occurring class D b-lactamase from Achromobacter xylosoxidans. Antimicrob Agents Chemother. 52:1952-1956.
21. Dray S, Dufour A-B. 2007. The ade4 package: implementing the duality diagram for ecologists. J Stat Soft. 22:20.
22. Dupont C, et al. 2015. Intrapatient diversity of Achromobacter spp. involved in chronic colonization of cystic fibrosis airways. Infect Genet Evol. 32:214-223.
23. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461.
24. Emerson J, Mcnamara S, Buccat AM, Worrell K, Burns JL. 2010. Changes in cystic fibrosis sputum microbiology in the United States between 1995 and 2008. Pediatr Pulmonol. 45:363-370.
25. Filkins LM, O'Toole GA. 2016. Cystic fibrosis lung infections: polymicrobial, complex, and hard to treat. Plos Pathog. 11:e1005258.
26. Freschi L, et al. 2015. Clinical utilization of genomics data produced by the international Pseudomonasaeruginosaconsortium. Front Microbiol. 6:8.
27. Frost LS, Leplae R, Summers AO, Toussaint A. 2005. Mobile genetic elements: The agents of open source evolution. Nat Rev Microbiol. 3:722- 732.
28. Fuchs TM, Eisenreich W, Heesemann J, Goebel W. 2012. Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- And intracellular habitats. FEMS Microbiol Rev. 36:435-462.
29. Glupczynski Y, Hansen W, Freney J, Yourassowsky E. 1988. In vitro susceptibility of Alcaligenes denitrificans subsp. xylosoxidans to 24 antimicrobial agents. Antimicrob Agents Chemother. 32:276-278.
30. Gross R, et al. 2008. The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae. BMC Genomics 9:449.
31. Günther F, Merle U, Frank U, Gaida MM, Mutters NT. 2016. Pseudobacteremia outbreak of biofilm-forming Achromobacter xylosoxidans - environmental transmission. BMC Infect Dis. 16:584.
32. Hansen CR, et al. 2010. Inflammation in Achromobacter xylosoxidans infected cystic fibrosis patients. J Cyst Fibros. 9:51-58.
33. Hansen CR, Pressler T, Ridderberg W, Johansen HK, Skov M. 2013. Achromobacter species in cystic fibrosis: cross-infection caused by indirect patient-to-patient contact. J Cystic Fibros. 12:609-615.
34. Hayat R, Ali S, Amara U, Khalid R, Ahmed I. 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol. 60:579-598.
35. Hu Y, et al. 2015. Genomic insights into intrinsic and acquired drug resistancemechanisms in Achromobacter xylosoxidans. Antimicrob Agents Chemother. 59:1152-1161.
36. Huson DH, Auch AF, Qi J, Schuster SC. 2007. MEGAN analysis of metagenomic data. Genome Res. 17:377-386.
37. Jakobsen TH, et al. 2013. Complete genome sequence of the cystic fibrosis pathogen Achromobacter xylosoxidans NH44784-1996 complies with important pathogenic phenotypes. Plos One 8:e68484.
38. Jeukens J, Freschi L, Kukavica-Ibrulj I, Nguyen D, Levesque RC. 2015. Draft genome sequence of triclosan-resistant cystic fibrosis isolate Achromobacter xylosoxidans CF304. Genome Announc. 3:0086500815.
39. Jolley KA. 2016. Achromobacter MLST website. Available from: http://pubmlst.org/achromobacter/.
40. Jombart T. 2008. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403-1405.
41. Konstantinidis KT, Tiedje JM. 2005. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci.102:2567-2572.
42. Kupfahl C, Walther M, Wendt C, Von Baum H. 2015. Identical Achromobacter strain in reusable surface disinfection tissue dispensers and a clinical isolate. Infect Control Hosp Epidemiol. 36:1362-1364.
43. Kurtz S, et al. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:30.
44. Lambiase A, et al. 2011. Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis. 30:973-980.
45. Land M, et al. 2015. Insights from 20 years of bacterial genome sequencing. Funct Integr Genomics 15:141-161.
46. Lewis K. 1994. Multidrug-resistance pumps in bacteria - variations on a theme. Trends Biochem Sci. 19:119-123.
47. Li X, et al. 2012. Genome sequence of the highly efficient arsenite-oxidizing bacterium Achromobacter arsenitoxydans SY8. J Bacteriol. 194:1243-1244.
48. Li X, Hu Y, Gong J, Zhang L, Wang G. 2013. Comparative genome characterization of Achromobacter members reveals potential genetic determinants facilitating the adaptation to a pathogenic lifestyle. Appl Microbiol Biotechnol. 97:6413-6425.
49. Lin HT, et al. 2009. MacB ABC transporter is a dimerwhose ATPase activity andmacrolide-binding capacity are regulated by themembrane fusion protein MacA. J Biol Chem. 284:1145-1154.
50. Linz B, et al. 2016. Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species. BMC Genomics 17:1-17.
51. Lipuma JJ. 2015. Assessing airway microbiota in cystic fibrosis: what more should be done? J Clin Microbiol. 53:2006-2007.
52. Loytynoja A. 2014. Phylogeny-aware alignment with PRANK. Methods Mol Biol. 1079:155-170.
53. Mcarthur AG, et al. 2013. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother. 57:3348-3357.
54. Melvin JA, Scheller EV, Miller JF, Cotter PA. 2014. Bordetella pertussis pathogenesis: currentandfuturechallenges. Nat Rev Microbiol.12:274-288.
55. Modali SD, Zgurskaya HI. 2011. The periplasmic membrane proximal domain of MacA acts as a switch in stimulation of ATP hydrolysis by MacB transporter. Mol Microbiol. 81:937-951.
56. Nguyen D, Singh PK. 2006. Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc Natl Acad Sci U S A. 103:8305-8306.
57. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304.
58. Olive AJ, Sassetti CM. 2016. Metabolic crosstalk between host and pathogen: sensing, adapting and competing. Nat Rev Microbiol. 14:221-234.
59. Papalia M, et al. 2013. OXA-258 from Achromobacter ruhlandii: a speciesspecific marker. J Clin Microbiol. 51:1602-1605.
60. Pederick VG, et al. 2014. Acquisition and role of molybdate in Pseudomonas aeruginosa. Appl Environ Microbiol. 80:6843-6852.
61. Perinet S, et al. 2016. Molybdate transporter ModABC is important for Pseudomonas aeruginosa chronic lung infection. BMC Res Notes 9:016-1840.
62. Pond SL, Frost SD, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
63. Ridderberg W, Bendstrup KE, Olesen HV, Jensen-Fangel S, Nørskov- Lauritsen N. 2011. Marked increase in incidence of Achromobacter xylosoxidans infections caused by sporadic acquisition from the environment. J Cyst Fibros. 10:466-469.
64. RidderbergW, Nielsen SM, Nørskov-Lauritsen N. 2015. Genetic adaptation of Achromobacter sp. during persistence in the lungs of cystic fibrosis patients. PLos One 10:e0136790.
65. Rohmer L, Hocquet D, Miller SI. 2011. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol. 19:341-348.
66. Rouli L, Merhej V, Fournier PE, Raoult D. 2015. The bacterial pangenome as a new tool for analysing pathogenic bacteria. N Microbes N Infect. 7:72-85.
67. SaierMH Jr, et al. 1998. Evolutionary origins ofmultidrug and drug-specific efflux pumps in bacteria. FASEB J. 12:265-274.
68. Saiman L, et al. 2001. Identification and antimicrobial susceptibility of Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. J Clin Microbiol. 39:3942-3945.
69. Schobert M, Jahn D. 2010. Anaerobic physiology of Pseudomonas aeruginosa in the cystic fibrosis lung. Int J Med Microbiol. 300:549-556.
70. Shannon P, et al. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13:2498- 2504.
71. Smith EE, et al. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci. 103:8487- 8492.
72. Smith MD, et al. 2015. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol Biol Evol. 32:1342-1353.
73. Spilker T, Vandamme P, Lipuma JJ. 2013. Identification and distribution of Achromobacter species in cystic fibrosis. J Cystic Fibros. 12:298-301.
74. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313.
75. Talbot NP, Flight WG. 2016. Severe Achromobacter xylosoxidans infection and loss of sputum bacterial diversity in an adult patient with cystic fibrosis. Paediatr Respir Rev. 20:27-29.
76. Tettelin H, Riley D, Cattuto C, Medini D. 2008. Comparative genomics: The bacterial pan-genome. Curr Opin Microbiol. 11:472-477.
77. Tom SK, Yau YCW, Beaudoin T, Lipuma JJ, Waters V. 2016. Effect of highdose antimicrobials on biofilm growth of Achromobacter species isolated from cystic fibrosis patients. Antimicrob Agents Chemother. 60:650-652.
78. Traglia G, et al. 2014. Presence of OXA-type enzymes in Achromobacter insuavis and A. dolens. Curr Microbiol. 69:501-506.
79. Traglia GM, et al. 2013. Distribution of allelic variants of the chromosomal gene bla OXA-114-like in Achromobacter xylosoxidans clinical isolates. Curr Microbiol. 67:596-600.
80. Trancassini M, et al. 2014. Outbreak of Achromobacter xylosoxidans in an Italian Cystic fibrosis centre: genome variability, biofilm production, antibiotic resistance, and motility in isolated strains. Front Microbiol. 5:8. doi:10.3389/fmicb.2014.00138.
81. Tritt A, Eisen JA, Facciotti MT, Darling AE. 2012. An integrated pipeline for de novo assembly of microbial genomes. Plos One 7:e42304.
82. Turton JF, et al. 2011. Identification of Achromobacter xylosoxidans by detection of the blaOXA-114-like gene intrinsic in this species. Diagn Microbiol Infect Dis. 70:408-411.
83. Vandamme P, et al. 2013. Classification of Achromobacter genogroups 2, 5, 7 and 14 as Achromobacter insuavis sp. nov., Achromobacter aegrifaciens sp. nov., Achromobacter anxifer sp. nov. and Achromobacter dolens sp. nov., respectively. Syst Appl Microbiol. 36:474-482.
84. Vargiu AV, Pos KM, Poole K, Nikaido H. 2016. Editorial: bad bugs in the XXIst century: resistance mediated by multi-drug efflux pumps in Gram-negative bacteria. Front Microbiol. 7:3.
85. Vincent AT, Derome N, Boyle B, Culley AI, Charette SJ. 2016. Next-generation sequencing (NGS) in the microbiological world: how to make the most of your money. J Microbiol Methods 16:30031-30038.
86. Wattam AR, et al. 2014. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 42:D581-D591.
87. Wolfgang MC, et al. 2003. Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci. 100:8484-8489.
88. Zelazny AM, et al. 2013. Adaptability and persistence of the emerging pathogen Bordetella petrii. Plos One 8:e65102.