Abstract
An arsenate susceptibility test was performed with transformed and cultured Escherichia coli DH5α cells, which carried recombinant DNA of full-length arsenic (ars) operon, namely a putative membrane permease, ArsP; a transcriptional repressor, ArsR; an arsenate reductase, ArsC; and an arsenical-resistance membrane transporter, Acr3, from the Japanese urease-positive thermophilic Campylobacter lari (UPTC) CF89-12. The E. coli DH5α transformant showed reduced susceptibility to arsenate (~1536 μg/mL), compared to the control. Thus, these ars four-genes from the UPTC CF89-12 strain cells could confer a reduced susceptibility to arsenate in the transformed and E. coli DH5α cells. E. coli transformants with truncated ars operons, acr3 (acr3) and arsC-acr3 (∆arsC-acr3), of the ars operon, showed an MIC value of 384 μg/mL (~384 μg/mL), similar to the E. coli cells which carried the pGEM-T vector (control). Reverse transcription PCR confirmed in vivo transcription of recombinant full-length ars operon and deletion variants (∆acr3 and ∆arsC-acr3) in the transformed E. coli cells.
Similar content being viewed by others
References
Butcher BG, Rawlings DE (2002) The divergent chromosomal ars operon of Acidithiobacillus ferrooxidans is regulated by an atypical ArsR protein. Microbiology 148:3983–3992
Butcher BG, Deane SM, Rawlings DE (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66:1826–1833
Cai J, Salmon K, DuBow MS (1998) A chromosomal ars operon homologue of Pseudomonas aeruginosa confers increased resistance to arsenic and antimony in Escherichia coli. Microbiology 144:2705–2713
Cervantes C, Ji G, Ramirez JL, Silver S (1994) Resistance to arsenic compounds in microorganisms. FEMS Microbiol Rev 15:355–367
Debruyne L, On SLW, De Brandt E, Vandamme P (2009) Novel Campylobacter lari-like bacteria from humans and molluscs: description of Campylobacter peloridis sp. nov., Campylobacter lari subsp. concheus subsp. nov. and Campylobacter lari subsp. lari subsp. nov. Int J Syst Evol Microbiol 59:1126–1132
Diorio C, Cai J, Marmor J, Shinder R, DuBow MS (1995) An Escherichia coli chromosomal ars operon homolog is functional in arsenic detoxification and is conserved in gram-negative bacteria. J Bacteriol 177:2050–2056
Harrington CS, Thomson-Carter FM, Carter PE (1997) Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme. J Clin Microbiol 35:2386–2392
Ji G, Silver S (1992a) Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J Bacteriol 174:3684–3694
Ji G, Silver S (1992b) Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci U S A 89:9474–9478
Lastovica AJ, Skirrow MB (2000) Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. coli. In: Nachamkin I, Blaser MJ (eds) Campylobacter. American Society for Microbiology, Washington DC, pp 89–120
Martinot M, Jaulhac B, Moog R, De Martino S, Kehrli P, Monteil H, Piemont Y (2001) Campylobacter lari bacteremia. Clin Microbiol Infect 7:96–97
Matsuda M, Kaneko A, Fukuyama M, Itoh T, Shingaki M, Inoue M, Moore JE, Murphy PG, Ishida Y (1996) First finding of urease-positive thermophilic strains of Campylobacter in river water in the Far East, namely, in Japan, and their phenotypic and genotypic characterization. J Appl Bacteriol 81:608–612
Miller WG, Wang G, Binnewies TT, Parker CT (2008) The complete genome sequence and analysis of the human pathogen Campylobacter lari. Foodborne Pathog Dis 5:371–386
Mobley HLT, Rosen BP (1982) Energetics of plasmid-mediated arsenate resistance in Escherichia coli. Proc Natl Acad Sci U S A 79:6119–6122
Nachamkin I, Stowell C, Skalina D, Jones AM, Hoop RM, Smibert RM (1984) Campylobacter laridis causing bacteremia in an immunosuppressed patient. Ann Intern Med 101:55–57
Nakajima T, Hayashi K, Nagatomi R, Nakanishi S, Matsubara K, Moore JE, Millar BC, Matsuda M (2013) Molecular identification and characterization of an arsenic four-gene operon in Campylobacter lari. Folia Microbiol 58:253–260
Nakanishi S, Nakajima T, Tazumi A, Katsubara K, Moore JE, Millar BC, Matsuda M (2013) Construction, expression and characterisation of recombinant DNAs of the urease gene operon from a urease-positive thermophilic Campylobacter (UPTC) isolate. Br J Biomed Sci 70:15–21
Noormohamed A, Fakhr MK (2013) Arsenic resistance and prevalence of arsenic resistance genes in Campylobacter jejuni and Campylobacter coli isolated from retail meats. Int J Environ Res Public Health 10(8):3453–3464
Qin J, Rosen BP, Zhang Y, Wang G, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci U S A 103:2075–2080
Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, NY
Sapkota AR, Price LB, Silbergeld EK, Schwab KJ (2006) Arsenic resistance in Campylobacter spp. isolated from retail poultry products. Appl Environ Microbiol 72:3069–3071
Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180:1655–1661
Shen Z, Han J, Wang Y, Sahin O, Zhang Q (2013) The contribution of arsB to arsenic resistance in Campylobacter jejuni. PLoS ONE 8(3):e58894
Shen Z, Luangtongkum T, Qiang Z, Jeon B, Wang L, Zhang Q (2014) Identification of a novel membrane transporter mediating resistance to organic arsenic in Campylobacter jejuni. Antimicrob Agents Chemother 58(4):2021–2029
Suzuki K, Wakao N, Kimura T, Sakka K, Ohmiya K (1998) Expression and regulation of the arsenic resistance operon of Acidiphilium multivorum AIU 301 plasmid pKW301 in Escherichia coli. Appl Environ Microbiol 64:411–418
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Wang L, Jeon B, Sahin O, Zhang Q (2009) Identification of an arsenic resistance and arsenic-sensing system in Campylobacter jejuni. Appl Environ Microbiol 75:5064–5073
Werno AM, Klena JD, Shaw GM, Murdoch DR (2002) Fatal case of Campylobacter lari prosthetic joint infection and bacteremia in an immunocompetent patient. J Clin Microbiol 40:1053–1055
Acknowledgments
This research was partially supported by a Grant-in-Aid for Scientific Research (C) (no. 20580346) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to MM). MM and JEM were funded through a Great Britain Sasakawa Foundation (Butterfield) Award to jointly examine the clinical significance of Campylobacter infection in the UK and Japan.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsuda, M., Kuribayashi, T., Yamamoto, S. et al. Transformation and characterization of an arsenic gene operon from urease-positive thermophilic Campylobacter (UPTC) in Escherichia coli . Folia Microbiol 61, 57–62 (2016). https://doi.org/10.1007/s12223-015-0405-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-015-0405-z