Skip to main content
SpringerLink
Log in

Unraveling the Amycolatopsis tucumanensis copper-resistome

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Heavy metal pollution is widespread causing serious ecological problems in many parts of the world; especially in developing countries where a budget for remediation technology is not affordable. Therefore, screening for microbes with high accumulation capacities and studying their stable resistance characteristics is advisable to define cost-effective any remediation strategies. Herein, the copper-resistome of the novel copper-resistant strain Amycolatopsis tucumanensis was studied using several approaches. Two dimensional gel electrophoresis revealed that proteins of the central metabolism, energy production, transcriptional regulators, two-component system, antioxidants and protective metabolites increased their abundance upon copper-stress conditions. Transcriptome analysis revealed that in presence of copper, superoxide dismutase, alkyl hydroperoxide reductase and mycothiol reductase genes were markedly induced in expression. The oxidative damage of protein and lipid from A. tucumanensis was negligible compared with that observed in the copper-sensitive strain Amycolatopsis eurytherma. Thus, we provide evidence that A. tucumamensis shows a high adaptation towards copper, the sum of which is proposed as the copper-resistome. This adaptation allows the strain to accumulate copper and survive this stress; besides, it constitutes the first report in which the copper-resistome of a strain of the genus Amycolatopsis with bioremediation potential has been evaluated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahn B, Cha J, Lee E, Han A, Thompson CJ, Roe J (2006) Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor. Mol Microbiol 59:1848–1858

    Article  PubMed  CAS  Google Scholar 

  • Albarracín VH, Winik B, Kothe E, Amoroso MJ, Abate CM (2008) Copper bioaccumulation by the actinobacterium Amycolatopsis sp. AB0. J Basic Microbiol 48:323–330

    Article  PubMed  Google Scholar 

  • Albarracín VH, Alonso-Vega P, Trujillo ME, Amoroso MJ, Abate CM (2010a) Amycolatopsis tucumanensis sp. nov., a novel copper resistant actinobacterium isolated from polluted sediments. Int J Syst Evol Microbiol 60:397–401

    Article  PubMed  Google Scholar 

  • Albarracín VH, Amoroso MJ, Abate CM (2010b) Bioaugmentation of copper polluted soil by Amycolatopsis tucumanensis to diminish phytoavailable copper for Zea mays plants. Chemosphere 79:131–137

    Article  PubMed  Google Scholar 

  • Alekshun MN, Levy SB (1999) The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol 7:410–413

    Article  PubMed  CAS  Google Scholar 

  • Alves AMCR, Euverink GJW, Santos H, Dijkhuizen L (2001) Different physiological roles of ATP- and PPi-Dependent phosphofructokinase isoenzymes in the methylotrophic actinomycete Amycolatopsis methanolica. J Bacteriol 183:7231–7240

    Article  PubMed  CAS  Google Scholar 

  • Benimeli CS, González AJ, Chaile AP, Amoroso MJ (2007) Temperature and pH effect on lindane removal by Streptomyces sp. M7 in soil extract. J Basic Microbiol 47:468–473

    Article  PubMed  CAS  Google Scholar 

  • Conrad CC, Choi J, Malakowsky CA, Talent JM, Dai R, Marshall P, Gracy RW (2001) Identification of protein carbonyls after two-dimensional electrophoresis. Proteomics 1:829–834

    Article  PubMed  CAS  Google Scholar 

  • Dávila Costa JS, Albarracín VH, Abate CM (2011a) Cupric reductase activity in copper-resistant Amycolatopsis tucumanensis. Water Air Soil Pollut 216:527–535

    Article  Google Scholar 

  • Dávila Costa JS, Albarracín VH, Abate CM (2011b) Responses of environmental Amycolatopsis strains to copper stress. Ecotoxicol Environ Saf 74:2020–2028

    Article  PubMed  Google Scholar 

  • Dupont CL, Grass G, Rensing C (2011) Copper toxicity and the origin of bacterial resistance—new insights and applications. Metallomics 11:1109–1118

    Article  Google Scholar 

  • Gallo G, Renzone G, Alduina R, Stegmann E, Weber T, Lantz AE, Thykaer J, Sangiorgi F, Scaloni A, Puglia AM (2010) Differential proteomic analysis reveals novel links between primary metabolism and antibiotic production in Amycolatopsis balhimycina. Proteomics 10:1336–1358

    Article  PubMed  CAS  Google Scholar 

  • Gudipaty SA, Larsen AS, Rensing C, McEvoy MM (2012) Regulation of Cu(I)/Ag(I) efflux genes in Escherichia coli by the sensor kinase CusS. FEMS Microbiol Lett 330:30–37. doi:10.1111/j.1574-6968.2012.02529.x

    Article  PubMed  CAS  Google Scholar 

  • Guimara BG, Souchon H, Honore N, Saint-Joanis B, Brosch R, Shepard W, Cole ST, Alzari PM (2005) Structure and mechanism of the alkyl hydroperoxidase AhpC, a key element of the Mycobacterium tuberculosis defense system against oxidative stress. J Biol Chem 280:25735–25742

    Article  Google Scholar 

  • Haferburg G, Groth I, Möllmann U, Kothe E, Sattler I (2009) Arousing sleeping genes: shifts in secondary metabolism of metal tolerant actinobacteria under conditions of heavy metal stress. Biometals 22(2):225–234

    Article  PubMed  CAS  Google Scholar 

  • Hamilton CJ, Finlay RMJ, Stewart MJG, Bonner A (2009) Mycothiol disulfide reductase: a continuous assay for slow time-dependent inhibitors. Anal Biochem 388:91–96

    Article  PubMed  CAS  Google Scholar 

  • Hellberg K, Grimsrud PA, Kruse AC, Banaszak LJ, Ohlendorf DH, Bernlohr DA (2010) X-ray crystallographic analysis of adipocyte fatty acid binding protein (aP2) modified with 4-hydroxy-2-nonenal. Protein Sci 19:1480–1489

    Article  PubMed  CAS  Google Scholar 

  • Hillas PJ, Soto del Alba F, Oyarzabal J, Wilks A, Ortiz de Montellano PR (2000) The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis. J Biol Chem 275:18801–18809

    Article  PubMed  CAS  Google Scholar 

  • Hillerich B, Westpheling J (2006) A new GntR family transcriptional regulator in Streptomyces coelicolor is required for morphogenesis and antibiotic production and controls transcription of an ABC transporter in response to carbon source. J Bacteriol 188:7477–7487

    Article  PubMed  CAS  Google Scholar 

  • Hong R, Kang TY, Michels CA, Gadura N (2012) Membrane lipid peroxidation in copper alloy-mediated contact killing of Escherichia coli. Appl Environ Microbiol 78(6):1776

    Article  PubMed  CAS  Google Scholar 

  • Hustavová H, Havraneková D (1997) The role of thiamine in Yersinia kristensenii resistance to antibiotics and heavy metals. Folia Microbiol (Praha) 42:569–573

    Article  Google Scholar 

  • Jeyakanthan J, Thamotharan S, Velmurugan D, Rao VSN, Nagarajan S, Shinkai A, Kuramitsue S, Yokoyamag S (2009) New structural insights and molecular-modelling studies of 4-methyl-5-β-hydroxyethylthiazole kinase from Pyrococcus horikoshii OT3 (PhThiK). Acta Cryst F65:978–986

    CAS  Google Scholar 

  • Joshi SG, Cooper M, Yost A, Paff M, Ercan UK, Fridman G, Friedman G, Fridman A, Brooks AD (2011) Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob Agents Chemother 55:1053–1062

    Article  PubMed  CAS  Google Scholar 

  • Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci 107:14373–14377

    Article  PubMed  CAS  Google Scholar 

  • Lemire J, Ryan Mailloux R, Auger C, Whalen D, Appanna VD (2010) Pseudomonas fluorescens orchestrates a fine metabolic-balancing act to counter aluminium toxicity. Environ Microbiol 12:1384–1390

    PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Macomber L, Imlay JA (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci 106(20):8344–8349

    Article  PubMed  CAS  Google Scholar 

  • Madeo M, O’Riordan N, Fuchs TM, Utratna M, Karatzas KAG, O’Byrne CP (2012) Thiamine plays a critical role in the acid tolerance of Listeria monocytogenes. FEMS Microbiol Lett 326:137–143

    Article  PubMed  CAS  Google Scholar 

  • Manteca A, Mäder U, Connolly BA, Sanchez J (2006) A proteomic analysis of Streptomyces coelicolor programmed cell death. Proteomics 6:6008–6022

    Article  PubMed  CAS  Google Scholar 

  • Mustroph A, Albrecht G, Hajirezaei M, Grimm B, Biemelt S (2005) Low levels of pyrophosphate in transgenic potato plants expressing E. coli pyrophosphatase lead to decreased vitality under oxygen deficiency. Ann Bot 96:717–726

    Article  PubMed  CAS  Google Scholar 

  • Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60

    Article  PubMed  CAS  Google Scholar 

  • Polti MA, Amoroso MJ, Abate CM (2007) Chromium (VI) resistance and removal by actinomycete strains isolated from sediments. Chemosphere 67:660–667

    Article  PubMed  CAS  Google Scholar 

  • Reeves RE, South DJ, Blytt HJ, Warren LG (1974) Pyrophosphate: d-fructose 6-phosphate 1-phosphotransferase. A new enzyme with the glycolytic function 6-phosphate 1-phosphotransferase. J Biol Chem 249:7737–7741

    PubMed  CAS  Google Scholar 

  • Reiß S, Pané-Farré J, Fuchs S, François P, Liebeke M, Schrenzel J, Lindequist U, Lalk M, Wolz C, Hecker M, Engelmann S (2012) Global analysis of the Staphylococcus aureus response to mupirocin. Antimicrob Agents Chemother 56:787–804

    Article  PubMed  Google Scholar 

  • Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213

    Article  PubMed  CAS  Google Scholar 

  • Sayre LM, Lin D, Yuan Q, Zhu X, Tang X (2006) Protein adducts generated from products of lipid oxidation: focus on HNE and one. Drug Metab Rev 38:651–675

    Article  PubMed  CAS  Google Scholar 

  • Seiler U, Pape H, Schröder W (1996) A pyrophosphate-dependent phosphofructokinase (PFK) from Actinoplanes sp., abstract 119. In: Abstracts of the VAAM meeting, Bayreuth

  • Seoane AS, Levy SB (1995) Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli. J Bacteriol 177:3414–3419

    PubMed  CAS  Google Scholar 

  • Sevcikova B, Rezuchova B, Homerova D, Kormanec J (2010) The Anti–Anti-Sigma factor BldG is involved in activation of the stress response sigma factor σH in Streptomyces coelicolor A3(2). J Bacteriol 192(21):5674–5681

    Article  PubMed  CAS  Google Scholar 

  • Shepard W, Haouz A, Graña M, Buschiazzo A, Betton JM, Cole ST, Alzari PM (2007) The crystal structure of Rv0813c from Mycobacterium tuberculosis reveals a new family of fatty acid-binding protein-like proteins in bacteria. J Bacteriol 189:1899–1904

    Article  PubMed  CAS  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215

    Article  PubMed  CAS  Google Scholar 

  • Stoyanov J, Hobman J, Brown N (2001) CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol Microbiol 39:502–512

    Article  PubMed  CAS  Google Scholar 

  • Vidali M (2001) Bioremediation an overview. Pure Appl Chem 73:1163–1172

    Article  CAS  Google Scholar 

  • Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226

    Article  PubMed  Google Scholar 

  • Wang G, Gong Y, Anderson J, Sun D, Minuk G, Roberts MS, Burczynski FJ (2005) Antioxidative function of L-FABP in L-FABP stably transfected Chang liver cells. Hepatology 42:871–879

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by CIUNT, FONCyT, CONICET, Argentina and DAAD, Germany. J.S.D.C. is supported by a CONICET doctoral scholarship. The authors thank greatly to Lic. María José Vildosa from CERELA-CONICET-TUCUMÁN for her valuable technical contribution in qRT-PCR.

Author information

Authors and Affiliations

  1. Pilot Plant of Industrial and Microbiological Processes (PROIMI), CONICET, Av. Belgrano y Pasaje Caseros, 4000, Tucumán, Argentina

    José Sebastián Dávila Costa, Carlos Mauricio Abate & María Julia Amoroso

  2. Institute of Microbiology, Friedrich-Schiller-University, 07743, Jena, Germany

    José Sebastián Dávila Costa & Erika Kothe

  3. Biochemistry, Chemistry and Pharmacy College, National University of Tucumán, 4000, Tucumán, Argentina

    Carlos Mauricio Abate & María Julia Amoroso

Authors
  1. José Sebastián Dávila Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erika Kothe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlos Mauricio Abate
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Julia Amoroso
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Julia Amoroso.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dávila Costa, J.S., Kothe, E., Abate, C.M. et al. Unraveling the Amycolatopsis tucumanensis copper-resistome. Biometals 25, 905–917 (2012). https://doi.org/10.1007/s10534-012-9557-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-012-9557-3

Keywords

Search

Navigation