Genes conferring copper resistance in Sinorhizobium meliloti CCNWSX0020 also promote the growth of Medicago lupulina in copper-contaminated soil

Applied and Environmental Microbiology

Volumn 80, Issue 6, 2014, Pages 1961-1971

  Li, Zhefei ^a   Ma, Zhanqiang ^a   Hao, Xiuli ^a   Rensing, Christopher ^b   Wei, Gehong ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MECHANISMS; COPPER ACCUMULATION; COPPER CONTAMINATION; COPPER-CONTAMINATED; METAL BINDING DOMAIN; OUTER MEMBRANE PROTEIN; REVERSE TRANSCRIPTASES; SINORHIZOBIUM MELILOTI;

BIOLOGICAL MEMBRANES; ENCODING (SYMBOLS); ESCHERICHIA COLI; GENE ENCODING; METAL IONS; SOIL POLLUTION; TAILINGS;

COPPER;

BACTERIUM; COPPER; GENE; GOLD MINE; GROWTH RATE; HOST PLANT; LEGUME; MEMBRANE; NODULATION; POLYMERASE CHAIN REACTION; PROTEIN; REAL TIME; ROOT; SOIL POLLUTION; TAILINGS;

COPPER;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; CHEMISTRY; CHINA; DNA SEQUENCE; DRUG EFFECT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEDICAGO; METABOLISM; MICROBIOLOGY; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINORHIZOBIUM MELILOTI; SOIL; SOIL POLLUTANT; TRANSPOSON;

CHINA; COPPER; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; GENE KNOCKOUT TECHNIQUES; GENES, BACTERIAL; MEDICAGO; MUTAGENESIS, INSERTIONAL; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SINORHIZOBIUM MELILOTI; SOIL; SOIL POLLUTANTS;

EID: 84897602334     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03381-13     Document Type: Article

References (52)

1. Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R, Fraser PE, Kruck T, von Bohlen A, Schulz-Schaeffer W, Giese A, Westaway D, Kretzschmar H. 1997. The cellular prion protein binds copper in vivo. Nature 390:684-687.
2. Van Assche F, Clusters H. 1990. Effect of metals on enzyme activity in plants. Plant Cell Environ. 13:195-206. http://dx.doi.org/10.1111/j.1365-3040.1990.tb01304.x.
3. Ebbs SD, Kochian LV. 1997. Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J. Environ. Qual. 26:776-781. http://dx.doi.org/10.2134/jeq1997.00472425002600030026x.
4. Leland HV, Carter JL. 1985. Effects of copper on production of periphyton, nitrogen fixation and processing of leaf litter in a Sierra Nevada, California, stream. Freshwater Biol. 15:155-173. http://dx.doi.org/10.1111/j.1365-2427.1985.tb00189.x.
5. Matuszewska E, Kwiatkowska J, Kuczynska-Wisnik D, Laskowska E. 2008. Escherichia coli heat-shock proteins IbpA/B are involved in resistance to oxidative stress induced by copper. Microbiology 154:1739-1747. http://dx.doi.org/10.1099/mic.0.2007/014696-0.
6. Munson GP, Lam DL, Outten FW, O'Halloran TV. 2000. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J. Bacteriol. 182:5864-5871. http://dx.doi.org/10.1128/JB.182.20.5864-5871.2000.
7. Grass G, Rensing C. 2001. Genes involved in copper homeostasis in Escherichia coli. J. Bacteriol. 183:2145-2147. http://dx.doi.org/10.1128/JB.183.6.2145-2147.2001.
8. Petersen C, Moller LB. 2000. Control of copper homeostasis in Escherichia coli by a P-type ATPase, CopA, and a MerR-like transcriptional activator, CopR. Gene 261:289-298. http://dx.doi.org/10.1016/S0378-1119(00)00509-6.
9. Kershaw CJ, Brown NL, Constantinidou C, Patel MD, Hobman JL. 2005. The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187-1198. http://dx.doi.org/10.1099/mic.0.27650-0.
10. Teitzel GM, Geddie A, De Long SK, Kirisits MJ, Whiteley M, Parsek MR. 2006. Survival and growth in the presence of elevated copper: transcriptional profiling of copper-stressed Pseudomonas aeruginosa. J. Bacteriol. 188:7242-7256. http://dx.doi.org/10.1128/JB.00837-06.
11. Ward SK, Hoye EA, Talaat AM. 2008. The global responses of Mycobacterium tuberculosis to physiological levels of copper. J. Bacteriol. 190: 2939-2946. http://dx.doi.org/10.1128/JB.01847-07.
12. Yang B, Shu WS, Ye ZH, Lan CY, Wong MH. 2003. Growth and metal accumulation in vetiver and two Sesbania species on lead/zinc mine tailings. Chemosphere 52:1593-1600. http://dx.doi.org/10.1016/S0045-6535(03)00499-5.
13. Jha PK, Nair S, Gopinathan MC, Babu CR. 1995. Suitability of rhizobiainoculated wild legumes Argyrolobium flaccidum, Astragalus graveolens, Indigofera gangetica and Lespedeza stenocarpa in providing a vegetational cover in an unreclaimed limestone quarry. Plant Soil 177:139-149. http://dx.doi.org/10.1007/BF00010120.
14. 2+. Int. Biodeter. Biodegr. 67:48-55. http://dx.doi.org/10.1016/j.ibiod.2011.10.008.
15. Ruiz-Diez B, Quinones MA, Fajardo S, Lopez MA, Higueras P, Fernandez-Pascual M. 2012. Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl. Microbiol. Biotechnol. 96:543-554. http://dx.doi.org/10.1007/s00253-011-3832-z.
16. Tittabutr P, Awaya JD, Li QX, Borthakur D. 2008. The cloned 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene from Sinorhizobium sp. strain BL3 in Rhizobium sp. strain TAL1145 promotes nodulation and growth of Leucaena leucocephala. Syst. Appl. Microbiol. 31:141-150. http://dx.doi.org/10.1016/j.syapm.2008.03.001.
17. Bianco C, Defez R. 2010. Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl. Environ. Microbiol. 76:4626-4632. http://dx.doi.org/10.1128/AEM.02756-09.
18. Li ZF, Ma ZQ, Hao XL, Wei GH. 2012. Draft genome sequence of Sinorhizobium meliloti CCNWSX0020, a nitrogen-fixing symbiont with copper tolerance capability isolated from lead-zinc mine tailings. J. Bacteriol. 194:1267-1268. http://dx.doi.org/10.1128/JB.06682-11.
19. Fan LM, Ma ZQ, Liang JQ, Li HF, Wang ET, Wei GH. 2011. Characterization of a copper-resistant symbiotic bacterium isolated from Medicago lupulina growing in mine tailings. Bioresour. Technol. 102:703-709. http://dx.doi.org/10.1016/j.biortech.2010.08.046.
20. Cheng GJ, Li YG, Zhou JC. 2006. Cloning and identification of opa22, a new gene involved in nodule formation by Mesorhizobium huakuii. FEMS Microbiol. Lett. 257:152-157. http://dx.doi.org/10.1111/j.1574-6968.2006.00158.x.
21. Wilson T, Carson J. 2001. Rapid, high-throughput extraction of bacterial genomic DNA from selective-enrichment culture media. Lett. Appl. Microbiol. 32:326-330. http://dx.doi.org/10.1046/j.1472-765X.2001.00906.x.
22. Kobori M, Nojima H. 1993. A simple treatment of DNA in a ligation mixture prior to electroporation improves transformation frequency. Nucleic Acids Res. 21:2782. http://dx.doi.org/10.1093/nar/21.11.2782.
23. Milcamps A, Ragatz DM, Lim P, Berger KA, de Bruijn FJ. 1998. Isolation of carbon-and nitrogen-deprivation-induced loci of Sinorhizobium meliloti 1021 by Tn5-luxAB mutagenesis. Microbiology 144:3205-3218. http://dx.doi.org/10.1099/00221287-144-11-3205.
24. Glickmann E, Dessaux Y. 1995. A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl. Environ. Microbiol. 61:793-796.
25. Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol. 26:192-195.
26. Wolk CP, Cai Y, Pano J. 1991. Use of a transposon with luciferase as a reporter to identify environmentally responsive genes in a cyanobacterium. Proc. Natl. Acad. Sci. U.S.A. 88:5355-5359. http://dx.doi.org/10.1073/pnas.88.12.5355.
27. Capela D, Barloy-Hubler F, Gouzy J, Bothe G, Ampe F, Batut J, Boistard P, Becker A, Boutry M, Cadieu E, Dréano S, Gloux S, Godrie T, Goffeau A, Kahn D, Kiss E, Lelaure V, Masuy D, Pohl T, Portetelle D, Pühler A, Purnelle B, Ramsperger U, Renard C, Thébault P, Vandenbol M, Weidner S, Galibert F. 2001. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl. Acad. Sci. U.S.A. 98:9877-9882. http://dx.doi.org/10.1073/pnas.161294398.
28. Wibberg D, Blom J, Jaenicke S, Kollin F, Rupp O, Scharf B, Schneiker-Bekel S, Sczcepanowski R, Goesmann A, Setubal JC, Schmitt R, Pühler A, Schlüter A. 2011. Complete genome sequencing of Agrobacterium sp. H13-3, the former Rhizobium lupini H13-3, reveals a tripartite genome consisting of a circular and a linear chromosome and an accessory plasmid but lacking a tumor-inducing Ti-plasmid. J. Biotechnol. 155:50-62. http://dx.doi.org/10.1016/j.jbiotec.2011.01.010.
29. Fraser JA, Davis MA, Hynes MJ. 2002. A gene from Aspergillus nidulans with similarity to URE2 of Saccharomyces cerevisiae encodes a glutathione S-transferase which contributes to heavy metal and xenobiotic resistance. Appl. Environ. Microbiol. 68:2802-2808. http://dx.doi.org/10.1128/AEM.68.6.2802-2808.2002.
30. Baker AJM, McGrath SP, Sidoli CMD, Reeves RD. 1994. The possibility of in situ heavy metal decontamination of polluted soils using crops of metal accumulating plants. Resour. Conserv. Recycl. 11:41-49. http://dx.doi.org/10.1016/0921-3449(94)90077-9.
31. Azadpour A, Matthews JE. 1996. Remediation of metal-contaminated sites using plants. Remediation 6:1-19. http://dx.doi.org/10.1002/rem.3440060302.
32. Mishra D, Kar M. 1974. Nickel in plant growth and metabolism. Bot. Rev. 40:395-452. http://dx.doi.org/10.1007/BF02860020.
33. Wallace A, Wallace GA, Cha JW. 1992. Some modifications in trace elements toxicities and deficiencies in plants resulting from interactions with other elements and chelating agents. The special case of iron. J. Plant Nutr. 15:1589-1598.
34. Reeve WG, Tiwari RP, Kale NB, Dilworth MJ, Glenn AR. 2002. ActP controls copper homeostasis in Rhizobium leguminosarum bv. viciae and Sinorhizobium meliloti preventing low pH-induced copper toxicity. Mol. Microbiol. 43:981-991. http://dx.doi.org/10.1046/j.1365-2958.2002.02791.x.
35. Tong L, Nakashima S, Shibasaka M, Katsuhara M, Kasamo K. 2002. A novel histidine-rich CPx-ATPase from the filamentous cyanobacterium Oscillatoria brevis related to multiple heavy metal cotolerance. J. Bacteriol. 184:5027-5035. http://dx.doi.org/10.1128/JB.184.18.5027-5035.2002.
36. Lin SJ, Culotta VC. 1995. The ATX1 gene of Saccharomyces cerevisiae encodes a small metal homeostasis factor that protects cells against reactive oxygen toxicity. Proc. Natl. Acad. Sci. U.S.A. 92:3784-3788. http://dx.doi.org/10.1073/pnas.92.9.3784.
37. Arguello JM. 2003. Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J. Membrane Biol. 195:93-108. http://dx.doi.org/10.1007/s00232-003-2048-2.
38. Haag AF, Wehmeier S, Beck S, Marlow VL, Fletcher V, James EK, Fergusonet GP. 2009. The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J. Bacteriol. 191:4681-4686. http://dx.doi.org/10.1128/JB.00318-09.
39. Ferguson GP, Datta A, Carlson RW, Walker GC. 2005. Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol. Microbiol. 56:68-80. http://dx.doi.org/10.1111/j.1365-2958.2005.04536.x.
40. Ardissone S, Kobayashi H, Kambara K, Rummel C, Noel KD, Walker GC, Broughton WJ, Deakin WJ. 2011. Role of BacA in lipopolysaccharide synthesis, peptide transport, and nodulation by Rhizobium sp. strain NGR234. J. Bacteriol. 193:2218-2228. http://dx.doi.org/10.1128/JB.01260-10.
41. Snyder S, Kim D, McIntosh TJ. 1999. Lipopolysaccharide bilayer structure: effect of chemotype, core mutations, divalent cations, and temperature. Biochemistry 38:10758-10767. http://dx.doi.org/10.1021/bi990867d.
42. Davies BW, Walker GC. 2007. Identification of novel Sinorhizobium meliloti mutants compromised for oxidative stress protection and symbiosis. J. Bacteriol. 189:2110-2113. http://dx.doi.org/10.1128/JB.01802-06.
43. Rossbach S, Mai DJ, Carter EL, Sauviac L, Capela D, Bruand C, Bruijn FJD. 2008. Response of Sinorhizobium meliloti to elevated concentrations of cadmium and zinc. Appl. Environ. Microbiol. 74:4218-4221. http://dx.doi.org/10.1128/AEM.02244-07.
44. Priefer UB. 1989. Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae VF39. J. Bacteriol. 171:6161-6168.
45. Perrine FM, Rolfe BG, Hynes MF, Hocart CH. 2004. Gas chromatography-mass spectrometry analysis of indoleacetic acid and tryptophan following aqueous chloroformate derivatisation of Rhizobium exudates. Plant Physiol. Biochem. 42:723-729. http://dx.doi.org/10.1016/j.plaphy.2004.07.008.
46. Fassler E, Evangelou MW, Robinson BH, Schulin R. 2010. Effects of indole-3-acetic acid (IAA) on sunflower growth and heavy metal uptake in combination with ethylene diamine disuccinic acid (EDDS). Chemosphere 80:901-907. http://dx.doi.org/10.1016/j.chemosphere.2010.04.077.
47. Choudhary SP, Oral HV, Bhardwaj R, Yu JQ, Tran LS. 2012. Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J. Exp. Bot. 63:5659-5675. http://dx.doi.org/10.1093/jxb/ers219.
48. Tassi E, Pouget J, Petruzzelli G, Barbafieri M. 2008. The effects of exogenous plant growth regulators in the phytoextraction of heavy metals. Chemosphere 71:66-73. http://dx.doi.org/10.1016/j.chemosphere.2007.10.027.
49. Dick GJ, Podell S, Johnson HA, Rivera-Espinoza Y, Bernier-Latmani R, McCarthy JK, Torpey JW, Clement BG, Gaasterland T, Tebo BM. 2008. Genomic insights into Mn(II) oxidation by the marine alphaproteobacterium Aurantimonas sp. strain SI85-9A1. Appl. Environ. Microbiol. 74: 2646-2658. http://dx.doi.org/10.1128/AEM.01656-07.
50. Glick BR, Penrose DM, Li J. 1998. A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J. Theor. Biol. 190:63-68. http://dx.doi.org/10.1006/jtbi.1997.0532.
51. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580. http://dx.doi.org/10.1016/S0022-2836(83)80284-8.
52. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol. 1:784-791. http://dx.doi.org/10.1038/nbt1183-784.