The soil microbiota harbors a diversity of carbapenem-hydrolyzing β-lactamases of potential clinical relevance

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 1, 2016, Pages 151-160

  Gudeta, Dereje Dadi ^a   Bortolaia, Valeria ^a   Amos, Greg ^b   Wellington, Elizabeth M H ^b   Brandt, Kristian K ^c   Poirel, Laurent ^d   Nielsen, Jesper Boye ^c   Westh, Henrik ^a,c   Guardabassi, Luca ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d University of Fribourg   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMPICILLIN; BETA LACTAMASE; CARBAPENEM; CARBAPENEMASE; CEFAZOLIN; CEFEPIME; CEFOTAXIME; CEFOXITIN; CEFPODOXIME; CEFTAZIDIME; CEFTRIAXONE; CLAVULANIC ACID; MEROPENEM; METALLO BETA LACTAMASE; PIPERACILLIN PLUS TAZOBACTAM; ANTIINFECTIVE AGENT; CARBAPENEM DERIVATIVE; RECOMBINANT PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CATALYSIS; CHRYSEOBACTERIUM; CHRYSEOBACTERIUM BALUSTINUM; CHRYSEOBACTERIUM PISCIUM; CHRYSEOBACTERIUM SCOPHTHALMUM; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; EPILITHONIMONAS LACTIS; EPILITHONIMONAS TENAX; ESCHERICHIA COLI; GENE FREQUENCY; GENE SEQUENCE; GENETIC VARIABILITY; GRAM NEGATIVE BACTERIUM; HETEROLOGOUS EXPRESSION; HOST RANGE; JANTHINOBACTERIUM; JANTHINOBACTERIUM LIVIDUM; MASSILIA OCULI; MASSILIA TIMONAE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEDOBACTER; PEDOBACTER AFRICANUS; PEDOBACTER AGRI; PEDOBACTER BOREALIS; PEDOBACTER BORYUNGENSIS; PEDOBACTER HEPARINUS; PEDOBACTER KYUNGHEENSIS; PEDOBACTER ROSEUS; PEDOBACTER SALTANS; PHENOTYPE; PRIORITY JOURNAL; PROPHAGE; SOIL MICROFLORA; SPHINGOMONAS; SPHINGOMONAS ADHAESIVA; SPHINGOMONAS AQUATILIS; SPHINGOMONAS ECHINOIDES; SPHINGOMONAS HANKOOKENSIS; SPHINGOMONAS JASPSI; SPHINGOMONAS MALTOPHILIA; SPHINGOMONAS PAUCIMOBILIS; AMINO ACID SEQUENCE; DRUG EFFECTS; ENZYMOLOGY; EUROPE; GENE EXPRESSION; GENETICS; HYDROLYSIS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CARBAPENEMS; CHRYSEOBACTERIUM; CLONING, MOLECULAR; ESCHERICHIA COLI; EUROPE; GENE EXPRESSION; HYDROLYSIS; MOLECULAR SEQUENCE DATA; PEDOBACTER; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SOIL MICROBIOLOGY; SPHINGOMONAS;

EID: 84957886265     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01424-15     Document Type: Article

References (54)

1. Wright GD. 2007. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175-186. http://dx.doi.org/10.1038/nrmicro1614.
2. D'Costa VM, McGrann KM, Hughes DW, Wright GD. 2006. Sampling the antibiotic resistome. Science 311:374-377. http://dx.doi.org/10.1126/science.1120800.
3. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111. http://dx.doi.org/10.1126/science.1220761.
4. Guardabassi L, Perichon B, van Heijenoort J, Blanot D, Courvalin P. 2005. Glycopeptide resistance vanA operons in Paenibacillus strains isolated from soil. Antimicrob Agents Chemother 49:4227-4233. http://dx.doi.org/10.1128/AAC.49.10.4227-4233.2005.
5. Humeniuk C, Arlet G, Gautier VP, Grimont RL, Philippon A. 2002. Beta-lactamases of Kluyvera ascorbata, probable progenitors of some plasmid-encoded CTX-M types. Antimicrob Agents Chemother 46:3045-3049. http://dx.doi.org/10.1128/AAC.46.9.3045-3049.2002.
6. Poirel L, Heritier C, Nordmann P. 2004. Chromosome-encoded Ambler class D beta-lactamase of Shewanella oneidensis as a progenitor of carbapenem-hydrolyzing oxacillinase. Antimicrob Agents Chemother 48:348-351. http://dx.doi.org/10.1128/AAC.48.1.348-351.2004.
7. Cornaglia G, Giamarellou H, Rossolini GM. 2011. Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect Dis 11:381-393. http://dx.doi.org/10.1016/S1473-3099(11)70056-1.
8. Galleni M, Lamotte-Brasseur J, Rossolini GM, Spencer J, Dideberg O, Frere JM, Metallo-beta-Lactamases Working Group. 2001. Standard numbering scheme for class B beta-lactamases. Antimicrob Agents Chemother 45:660-663. http://dx.doi.org/10.1128/AAC.45.3.660-663.2001.
9. Queenan AM, Bush K. 2007. Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 20:440-458. http://dx.doi.org/10.1128/CMR.00001-07.
10. Bebrone C, Delbruck H, Kupper MB, Schlomer P, Willmann C, Frere JM, Fischer R, Galleni M, Hoffmann KM. 2009. The structure of the di-zinc subclass B2 metallo-beta-lactamase CphA reveals that the second inhibitory zinc ion binds in the histidine site. Antimicrob Agents Chemother 53:4464-4471. http://dx.doi.org/10.1128/AAC.00288-09.
11. Fonseca F, Bromley EH, Saavedra MJ, Correia A, Spencer J. 2011. Crystal structure of Serratia fonticola Sfh-I: activation of the nucleophile in mono-zinc metallo-beta-lactamases. J Mol Biol 411:951-959. http://dx.doi.org/10.1016/j.jmb.2011.06.043.
12. Nordmann P, Naas T, Poirel L. 2011. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 17:1791-1798. http://dx.doi.org/10.3201/eid1710.110655.
13. Wachino J, Yoshida H, Yamane K, Suzuki S, Matsui M, Yamagishi T, Tsutsui A, Konda T, Shibayama K, Arakawa Y. 2011. SMB-1, a novel subclass B3 metallo-beta-lactamase, associated with ISCR1 and a class 1 integron, from a carbapenem-resistant Serratia marcescens clinical isolate. Antimicrob Agents Chemother 55:5143-5149. http://dx.doi.org/10.1128/AAC.05045-11.
14. Pollini S, Maradei S, Pecile P, Olivo G, Luzzaro F, Docquier JD, Rossolini GM. 2013. FIM-1, a new acquired metallo-beta-lactamase from a Pseudomonas aeruginosa clinical isolate from Italy. Antimicrob Agents Chemother 57:410-416. http://dx.doi.org/10.1128/AAC.01953-12.
15. Ashbolt NJ, Amezquita A, Backhaus T, Borriello P, Brandt KK, Collignon P, Coors A, Finley R, Gaze WH, Heberer T, Lawrence JR, Larsson DG, McEwen SA, Ryan JJ, Schonfeld J, Silley P, Snape JR, Van den Eede C, Topp E. 2013. Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ Health Perspect 121:993-1001. http://dx.doi.org/10.1289/ehp.1206316.
16. Martínez JL, Coque TM, Baquero F. 2015. What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol 13:116-123. http://dx.doi.org/10.1038/nrmicro3399.
17. Poulsen PH, Al-Soud WA, Bergmark L, Magid J, Hansen LH, Sørensen SJ. 2013. Effects of fertilization with urban and agricultural organic wastes in a field trial - prokaryotic diversity investigated by pyrosequencing. Soil Biol Biochem 57:784-793. http://dx.doi.org/10.1016/j.soilbio.2011.12.023.
18. Berg J, Thorsen MK, Holm PE, Jensen J, Nybroe O, Brandt KK. 2010. Cu exposure under field conditions co-selects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ Sci Technol 44:8724-8728. http://dx.doi.org/10.1021/es101798r.
19. Brandt KK, Petersen A, Holm PE, Nybroe O. 2006. Decreased abundance and diversity of culturable Pseudomonas spp. populations with increasing copper exposure in the sugar beet rhizosphere. FEMS Microbiol Ecol 56:281-291. http://dx.doi.org/10.1111/j.1574-6941.2006.00081.x.
20. Petersen SO, Henriksen K, Mortensen G, Krogh P, Brandt KK, Sørensen J, Madsen T, Petersen J, Grøn C. 2003. Recycling of sewage sludge and household compost to arable land: fate and effects of organic contaminants, and impact on soil fertility. Soil Till Res 72:139-152. http://dx.doi.org/10.1016/S0167-1987(03)00084-9.
21. Pontiroli A, Travis ER, Sweeney FP, Porter D, Gaze WH, Mason S, Hibberd V, Holden J, Courtenay O, Wellington EMH. 2011. Pathogen quantitation in complex matrices: a multi-operator comparison of DNA extraction methods with a novel assessment of PCR inhibition. PLoS One 6:e17916. http://dx.doi.org/10.1371/journal.pone.0017916.
22. Selama O, Amos GC, Djenane Z, Borsetto C, Laidi RF, Porter D, Nateche F, Wellington EMH, Hacène H. 2014. Screening for genes coding for putative antitumor compounds, antimicrobial and enzymatic activities from haloalkalitolerant and haloalkaliphilic bacteria strains of Algerian Sahara soils. Biomed Res Int 2014:317524. http://dx.doi.org/10.1155/2014/317524.
23. Tolba S, Egan S, Kallifidas D, Wellington EMH. 2002. Distribution of streptomycin resistance and biosynthesis genes in streptomycetes recovered from different soil sites. FEMS Microbiol Ecol 42:269-276. http://dx.doi.org/10.1111/j.1574-6941.2002.tb01017.x.
24. Nordmann P, Gniadkowski M, Giske CG, Poirel L, Woodford N, Miriagou V. 2012. Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect 18:432-438. http://dx.doi.org/10.1111/j.1469-0691.2012.03815.x.
25. Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M. 2002. Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68:2391-2396. http://dx.doi.org/10.1128/AEM.68.5.2391-2396.2002.
26. Dortet L, Bréchard L, Cuzon G, Poirel L, Nordmann P. 2014. Strategy for rapid detection of carbapenemase-producing Enterobacteriaceae. Antimicrob Agents Chemother 58:2441-2445. http://dx.doi.org/10.1128/AAC.01239-13.
27. Stackebrandt E, Goebel BM. 1994. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846-849. http://dx.doi.org/10.1099/00207713-44-4-846.
28. Rossolini GM, Condemi MA, Pantanella F, Docquier JD, Amicosante G, Thaller MC. 2001. Metallo-β-lactamase producers in environmental microbiota: new molecular class B enzyme in Janthinobacterium lividum. Antimicrob Agents Chemother 45:837-844. http://dx.doi.org/10.1128/AAC.45.3.837-844.2001.
29. Newman JR, Fuqua C. 1999. Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227:197-203. http://dx.doi.org/10.1016/S0378-1119(98)00601-5.
30. Poirel L, Rodriguez-Martinez JM, Al Naiemi N, Debets-Ossenkopp YJ, Nordmann P. 2010. Characterization of DIM-1, an integron-encoded metallo-beta-lactamase from a Pseudomonas stutzeri clinical isolate in The Netherlands. Antimicrob Agents Chemother 54:2420-2424. http://dx.doi.org/10.1128/AAC.01456-09.
31. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain JM. 2014. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212-220. http://dx.doi.org/10.1128/AAC.01310-13.
32. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4:363-371. http://dx.doi.org/10.1038/nprot.2009.2.
33. Dortet L, Poirel L, Nordmann P. 2012. Rapid detection of carbapenemase-producing Pseudomonas spp. J Clin Microbiol 50:3773-3776. http://dx.doi.org/10.1128/JCM.01597-12.
34. Bellais S, Aubert D, Naas T, Nordmann P. 2000. Molecular and biochemical heterogeneity of class B carbapenem-hydrolyzing beta-lactamases in Chryseobacterium meningosepticum. Antimicrob Agents Chemother 44:1878-1886. http://dx.doi.org/10.1128/AAC.44.7.1878-1886.2000.
35. Docquier JD, Pantanella F, Giuliani F, Thaller MC, Amicosante G, Galleni M, Frere JM, Bush K, Rossolini GM. 2002. CAU-1, a subclass B3 metallo-beta-lactamase of low substrate affinity encoded by an ortholog present in the Caulobacter crescentus chromosome. Antimicrob Agents Chemother 46:1823-1830. http://dx.doi.org/10.1128/AAC.46.6.1823-1830.2002.
36. Yong D, Toleman MA, Bell J, Ritchie B, Pratt R, Ryley H, Walsh TR. 2012. Genetic and biochemical characterization of an acquired subgroup B3 metallo-beta-lactamase gene, blaAIM-1 , and its unique genetic context in Pseudomonas aeruginosa from Australia. Antimicrob Agents Chemother 56:6154-6159. http://dx.doi.org/10.1128/AAC.05654-11.
37. Voha C, Docquier JD, Rossolini GM, Fosse T. 2006. Genetic and biochemical characterization of FUS-1 (OXA-85), a narrow-spectrum class D beta-lactamase from Fusobacterium nucleatum subsp. polymorphum. Antimicrob Agents Chemother 50:2673-2679. http://dx.doi.org/10.1128/AAC.00058-06.
38. Naas T, Bellais S, Nordmann P. 2003. Molecular and biochemical characterization of a carbapenem-hydrolysing beta-lactamase from Flavobacterium johnsoniae. J Antimicrob Chemother 51:267-273. http://dx.doi.org/10.1093/jac/dkg069.
39. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. 2009. Functional metagenomics reveals diverse β-lactamases in a remote Alaskan soil. ISME J 3:243-251. http://dx.doi.org/10.1038/ismej.2008.86.
40. Lisa M, Morán-Barrio J, Guindón M, Vila AJ. 2012. Probing the role of Met221 in the unusual metallo-β-lactamase GOB-18. Inorg Chem 51:12419-12425. http://dx.doi.org/10.1021/ic301801h.
41. Aksyuk AA, Leiman PG, Kurochkina LP, Shneider MM, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG. 2009. The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J 28:821-829. http://dx.doi.org/10.1038/emboj.2009.36.
42. Kostyuchenko VA, Leiman PG, Chipman PR, Kanamaru S, van Raaij MJ, Arisaka F, Mesyanzhinov VV, Rossmann MG. 2003. Three-dimensional structure of bacteriophage T4 baseplate. Nat Struct Biol 10:688-693. http://dx.doi.org/10.1038/nsb970.
43. Chandler M, de la Cruz F, Dyda F, Hickman AB, Moncalian G, Ton-Hoang B. 2013. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat Rev Microbiol 11:525-538. http://dx.doi.org/10.1038/nrmicro3067.
44. Colomer-Lluch M, Jofre J, Muniesa M. 2011. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6:e17549. http://dx.doi.org/10.1371/journal.pone.0017549.
45. Balcazar JL. 2014. Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog 10:e1004219. http://dx.doi.org/10.1371/journal.ppat.1004219.
46. Zhang W, Fisher JF, Mobashery S. 2009. The bifunctional enzymes of antibiotic resistance. Curr Opin Microbiol 12:505-511. http://dx.doi.org/10.1016/j.mib.2009.06.013.
47. Garcia-Sáez I, Mercuri P, Papamicael C, Kahn R, Frere J, Galleni M, Rossolini GM, Dideberg O. 2003. Three-dimensional structure of FEZ-1, a monomeric subclass B3 metallo-β-lactamase from Fluoribacter gormanii, in native form and in complex with D-captopril. J Mol Biol 325:651-660. http://dx.doi.org/10.1016/S0022-2836(02)01271-8.
48. Dortet L, Nordmann P, Poirel L. 2012. Association of the emerging carbapenemase NDM-1 with a bleomycin resistance protein in Enterobacteriaceae and Acinetobacter baumannii. Antimicrob Agents Chemother 56:1693-1697. http://dx.doi.org/10.1128/AAC.05583-11.
49. NDM-1-positive Enterobacteriaceae. Antimicrob Agents Chemother 55:5403-5407. http://dx.doi.org/10.1128/AAC.00585-11.
50. VIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother 43:1584-1590.
51. Poirel L, Naas T, Nicolas D, Collet L, Bellais S, Cavallo JD, Nordmann P. 2000. Characterization of VIM-2, a carbapenem-hydrolyzing metallobeta-lactamase and its plasmid- and integron-borne gene from a Pseudomonas aeruginosa clinical isolate in France. Antimicrob Agents Chemother 44:891-897. http://dx.doi.org/10.1128/AAC.44.4.891-897.2000.
52. Gibb AP, Tribuddharat C, Moore RA, Louie TJ, Krulicki W, Livermore DM, Palepou MF, Woodford N. 2002. Nosocomial outbreak of carbapenem-resistant Pseudomonas aeruginosa with a new bla(IMP) allele, bla(IMP-7). Antimicrob Agents Chemother 46:255-258. http://dx.doi.org/10.1128/AAC.46.1.255-258.2002.
53. Nordmann P, Dortet L, Poirel L. 2012. Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol Med 18:263-272. http://dx.doi.org/10.1016/j.molmed.2012.03.003.
54. Matsumura N, Minami S, Watanabe Y, Iyobe S, Mitsuhashi S. 1999. Role of permeability in the activities of beta-lactams against gram-negative bacteria which produce a group 3 beta-lactamase. Antimicrob Agents Chemother 43:2084-2086.