Abstract
Arthrobacter sp. are Gram-positive bacilli commonly obtained from soil and in the hospital environment. These species have been reported to cause several types of infection. Heavy metals are a threat to the ecological system due to their high-levels of toxicity and the fluoroquinolones are antimicrobials widely used for the treatment of different bacterial infections. The aim of this study was to investigate the resistance to fluoroquinolone and heavy metals, the presence of plasmid-mediated resistance (PMQR) genes and heavy metals resistance (HMR) genes and the presence of plasmids in Arthrobacter sp. obtained from Brazilian soils. Bacterial isolation was performed using soil samples from different Brazilian regions. The bacterial identification was performed by 16S rRNA gene sequencing. The resistance profile for fluoroquinolones and heavy metals was determined by MIC. Several PMQR and HMR genes and plasmid families were investigated by PCR. Eight isolates were obtained from soil samples from different cultivations and regions of Brazil. All isolates were resistant to all fluoroquinolones, cadmium, cobalt and zinc and the majority to copper. Among the PMQR genes, the qepA (4) was the most prevalent, followed by qnrS (3), qnrB (3), oqxB (2) and oqxA (1). Among the HMR genes, the copA was detected in all isolates and the czcA in two isolates. The replication origin of the ColE-like plasmid was detected in all isolates; however, no plasmid was detected by extraction. The association of resistance to heavy metals and antimicrobials is a threat to the environmental balance and to human health. There are no studies reporting the association of PMQR and HMR genes in bacteria belonging to the genus Arthrobacter. To the best of our knowledge, this is the first report of qnrB, qepA, oqxA and oqxB in Arthrobacter species.
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References
Adarsh VK, Mishra M, Chowdhyry S, Sudarshan M, Thakur AR, Chaudhuri SR (2007) Studies on metal microbe interaction of three bacterial isolates from east Calcutta wetland. J Biol Sci 7:80–88. https://doi.org/10.3844/ojbsci.2007.80.88
Altimira F, Yáñez C, Bravo G, González M, Rojas LA, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:193. https://doi.org/10.1186/1471-2180-12-193
Bafana A, Krishnamurthi K, Patil M, Chakrabarti T (2010) Heavy metal resistance in Arthrobacter ramosus strain G2 isolated from mercuric salt-contaminated soil. J Hazard Mater 177:416–481. https://doi.org/10.1016/j.jhazmat.2009.12.058
Bernasconi E, Valsangiacomo C, Peduzzi R, Carota A, Moccetti T, Funke G (2004) Arthrobacter woluwensis subacute infective endocarditis: case report and review of the literature. Clin Infect Dis 38:e27–e31. https://doi.org/10.1086/381436
Blondeau JM (2004) Fluoroquinolones: mechanism of action, classification, and development of resistance. Surv Ophthalmol 49(Suppl2):S73–78. https://doi.org/10.1016/j.survophthal.2004.01.005
Bouskill NJ, Barnhart EP, Galloway TS, Handy RD, Ford TE (2007) Quantification of changing Pseudomonas aeruginosa sodA, htpX and mt gene abundance in response to trace metal toxicity: a potential in situ biomarker of environmental health. FEMS Microbiol Ecol 60:276–286. https://doi.org/10.1111/j.1574-6941.2007.00296.x
Brandsch R, Decker K (1984) Isolation and partial characterization of plasmid DNA from Arthrobacter oxidans. Arch Microbiol 138:15–17
Buschmann AH, Tomova A, López A, Maldonado MA, Henríquez LA, Ivanova L et al (2012) Salmon aquaculture and antimicrobial resistance in the marine environment. PLoS One 7:e42724. https://doi.org/10.1371/journal.pone.0042724
Cacciari I, Lippi D (1987) Arthrobacters: successful arid soil bacteria: a review. Arid Land Res Manag 1:1–30
Carattoli A (2013) Plasmids and the spread of resistance. Int J Med Microbiol 303:298–304. https://doi.org/10.1016/j.ijmm.2013.02.001
Carattoli A, Bertini A, Villa L, Hopkins KL, Threlfall EJ (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228. https://doi.org/10.1016/j.mimet.2005.03.018
Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60:394–397. https://doi.org/10.1093/jac/dkm204
Chen X, Zhang W, Pan W, Yin J, Pan Z, Gao S, Jiao X (2012) Prevalence of qnr, aac(6′)-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob Agents Chemother 56:3423–3427. https://doi.org/10.1128/AAC.06191-11
CLSI (2015) Performance standards for antimicrobial susceptibility testing: twenty-fifth informational supplement. CLSI document M100-S25. Wayne, PA: Clinical and Laboratory Standards Institute; 2015
Deredjian A, Colinon C, Brothier E, Favre-Bonté S, Cournoyer B, Nazaret S (2011) Antibiotic and metal resistance among hospital and outdoor strains of Pseudomonas aeruginosa. Res Microbiol 162:689–700. https://doi.org/10.1016/j.resmic.2011.06.007
Dsouza M, Taylor MW, Turner SJ, Aislabie J (2005) Genomic and phenotypic insights into the ecology of Arthrobacter from Antarctic soils. BMC Genom 16:36. https://doi.org/10.1186/s12864-015-1220-2
Fredrickson JK, Zachara JM, Balkwill DL, Kennedy D, Li SW, Kostandarithes HM et al (2004) Geomicrobiology of high-level nuclear waste-contaminated vadose sediments at the Hanford site, Washington state. Appl Environ Microbiol 70:4230–4241. https://doi.org/10.1128/AEM.70.7.4230-4241.2004
Funke G, Pagano-Niederer M, Sjödén B, Falsen E (1988) Characteristics of Arthrobacter cumminsii, the most frequently encountered Arthrobacter species in human clinical specimens. J Clin Microbiol 36:1539–1543
García-Fernández A, Fortini D, Veldman K, Mevius D, Carattoli A (2009) Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 63:274–281. https://doi.org/10.1093/jac/dkn470
Hawkey PM (2003) Mechanisms of quinolone action and microbial response. J Antimicrob Chemother 51(Suppl1):29–35. https://doi.org/10.1093/jac/dkg207
Heidorn T, Camsund D, Huang H-H, Lindberg P, Oliveira P, Stensjö K, Lindblad P (2011) Chapter twenty-four-synthetic biology in cyanobacteria: engineering and analyzing novel functions. Methods Enzymol 497:539–579. https://doi.org/10.1016/B978-0-12-385075-1.00024-X
Imirzalioglu C, Hain T, Hossain H, Chakraborty T, Domann E (2010) Erythema caused by a localised skin infection with Arthrobacter mysorens. BMC Infect Dis 10:352. https://doi.org/10.1186/1471-2334-10-352
Jacoby GA (2005) Mechanisms of resistance to quinolones. Clin Infect Dis 41(Suppl2):S120-6. https://doi.org/10.1086/428052
Karczmarczyk M, Abbott Y, Walsh C, Leonard N, Fanning S (2001) Characterization of multidrug-resistant Escherichia coli isolates from animals presenting at a university veterinary hospital. Appl Environ Microbiol 77:7104–7112. https://doi.org/10.1128/AEM.00599-11
Kim G-Y, Suh J-T, Choi S-K, Lee H-J (2007) A Case of Bacteremia Caused by Arthrobacter woluwensis. Korean J Clin Microbiol 10:160–163
Mages IS, Frodl R, Bernard KA, Funke G (2008) Identities of Arthrobacter spp. and Arthrobacter-like bacteria encountered in human clinical specimens. J Clin Microbiol 46:2980–2986. https://doi.org/10.1128/JCM.00658-08
Margesin R, Schinner F (1997) Heavy metal resistant Arthrobacter sp.: a tool for studying conjugational plasmid transfer between gram-negative and gram-positive bacteria. J Basic Microbiol 37:217–227
Mukherjee K, Tribedi P, Chowdhury A, Ray T, Joardar A, Giri S, Sil AK (2011) Isolation of a Pseudomonas aeruginosa strain from soil that can degrade polyurethane diol. Biodegradation 22:377–388. https://doi.org/10.1007/s10532-010-9409-1
Park CH, Han MS, Kim JK, Jeong SJ, Ku NS, Kim H (2012) Development of Arthrobacter woluwensis bacteremia in a patient with multiple myeloma: a case report and comprehensive literature review. Infect Chemother 44:205–209. https://doi.org/10.3947/ic.2012.44.3.205
Raja CE, Selvam GS (2009) Plasmid profile and curing analysis of Pseudomonas aeruginosa as metal resistant. Int J Environ Sci Technol 6:259–266. https://doi.org/10.1007/BF03327630
Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213
Rodríguez-Martínez JM, Velasco C, Briales A, García I, Conejo MC, Pascual A (2008) Qnr-like pentapeptide repeat proteins in gram-positive bacteria. J Antimicrob Chemother 61:1240–1243. https://doi.org/10.1093/jac/dkn115
Sarma B, Axharya C, Joshi SR (2010) Pseudomonads: a versatile bacterial group exhibiting dual resistance to metals and antibiotics. Afr J Microbiol Res 4:2828–2835
Tomova A, Ivanova L, Buschmann AH, Rioseco ML, Kalsi RK, Godfrey HP, Cabello FC (2015) Antimicrobial resistance genes in marine bacteria and human uropathogenic Escherichia coli from a region of intensive aquaculture. Environ Microbiol Rep 7:803–809. https://doi.org/10.1111/1758-2229.12327
Tomova A, Ivanova L, Buschmann AH, Godfrey HP, Cabello FC (2018) Plasmid-mediated quinolone resistance (PMQR) genes and class 1 integrons in quinolone-resistant marine bacteria and clinical isolates of Escherichia coli from an aquacultural area. Microb Ecol 75:104–112. https://doi.org/10.1007/s00248-017-1016-9
Weisburg WG, Barns SM, Pelletier BA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
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This work was supported by São Paulo Research Foundation—FAPESP [Grant Number 2015/18990-2].
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IFLG, JPRF, DGS and EGS performed the laboratory work and analyzed the results; EGS supervised the work; IFLG and EGS wrote the paper.
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Gallo, I.F.L., Furlan, J.P.R., Sanchez, D.G. et al. Heavy metal resistance genes and plasmid-mediated quinolone resistance genes in Arthrobacter sp. isolated from Brazilian soils. Antonie van Leeuwenhoek 112, 1553–1558 (2019). https://doi.org/10.1007/s10482-019-01281-9
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DOI: https://doi.org/10.1007/s10482-019-01281-9