Skip to main content
SpringerLink
Log in

Association between gentamicin resistance and stress tolerance in water isolates of Ralstonia pickettii and R. mannitolilytica

  • Original Article
  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Members of the species Ralstonia pickettii and R. mannitolilytica, although ubiquitous and lacking major virulence factors, have been associated with nosocomial outbreaks. Tolerance to metals, antibiotics, and disinfectants may represent an advantage for their ubiquity and opportunistic pathogenic potential. In this study, we compared five strains that differed on the origin (hospital effluent, tap water, mineral water) and in the susceptibility to aminoglycosides, regarding their tolerance to metals and disinfection. The growth kinetics and biofilm formation capacity were tested in four R. pickettii strains and one R. mannitolilytica at sub-inhibitory concentrations of aminoglycosides or arsenite. The survival to UV radiation, chlorine, or hydrogen peroxide was also compared in aminoglycoside resistant and susceptible strains. Aminoglycoside-resistant strains presented a higher tolerance to arsenite than the susceptible ones and either aminoglycosides or arsenite was observed to stimulate the biofilm formation. Sub-inhibitory concentrations of the aminoglycoside gentamicin or arsenite significantly decreased the growth rate and yield, but only arsenite caused a significant increase of the lag phase. Hydrogen peroxide presented higher disinfection effectiveness against aminoglycoside susceptible than against resistant strains, an effect that was not observed for UV or chlorine. Although this conclusion needs validation based on a larger number of isolates, including clinical, the results suggest that aminoglycoside resistance may be associated with traits that influence Ralstonia spp. fitness in the environment.

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

Similar content being viewed by others

References

  • Adley C, Ryan M, Pembroke J, Saieb F (2005) Ralstonia pickettii: biofilm formation in high-purity water. Biofilms: Persistence and Ubiquity, pp 261–271

  • Ahemad M, Malik A (2013) Prevalence of heavy metal and antibiotic resistance in bacterial isolates from metal polluted soils. Microbiol J. https://doi.org/10.3923/mj.2013

  • Aka ST, Haji SH (2015) Sub-MIC of antibiotics induced biofilm formation of Pseudomonas aeruginosa in the presence of chlorhexidine. Braz J Microbiol 46:149–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson RL, Holland BW, Carr JK, Bond WW, Favero MS (1990) Effect of disinfectants on pseudomonads colonized on the interior surface of PVC pipes. Am J Public Health 80:17–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48(Suppl 1):5–16

    Article  CAS  PubMed  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    Article  CAS  PubMed  Google Scholar 

  • Balaban N (2008) Control of biofilm infections by signal manipulation vol 2. Springer

  • Becerra-Castro C, Machado RA, Vaz-Moreira I, Manaia CM (2015) Assessment of copper and zinc salts as selectors of antibiotic resistance in Gram-negative bacteria. Sci Total Environ 530-531:367–372

    Article  CAS  PubMed  Google Scholar 

  • Boutros N, Gonullu N, Casetta A, Guibert M, Ingrand D, Lebrun L (2002) Ralstonia pickettii traced in blood culture bottles. J Clin Microbiol 40:2666–2667

    Article  PubMed  PubMed Central  Google Scholar 

  • CLSI (2015) Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement M100-S25. vol 35. Clinical and Laboratory Standards Institute, USA

  • Coenye T, Vandamme P, LiPuma JJ (2002) Infection by Ralstonia species in cystic fibrosis patients: identification of R. pickettii and R. mannitolilytica by polymerase chain reaction. Emerg Infect Dis 8:692–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coman I, Bilodeau L, Lavoie A, Carricart M, Tremblay F, Zlosnik JE, Berthiaume Y (2017) Ralstonia mannitolilytica in cystic fibrosis: a new predictor of worse outcomes. Respir Med Case Rep 20:48–50

    CAS  PubMed  Google Scholar 

  • Daxboeck F, Stadler M, Assadian O, Marko E, Hirschl AM, Koller W (2005) Characterization of clinically isolated Ralstonia mannitolilytica strains using random amplification of polymorphic DNA (RAPD) typing and antimicrobial sensitivity, and comparison of the classification efficacy of phenotypic and genotypic assays. J Med Microbiol 54:55–61

    Article  CAS  PubMed  Google Scholar 

  • De Baere T et al (2001) Classification of Ralstonia pickettii biovar 3/'thomasii'strains (Pickett 1994) and of new isolates related to nosocomial recurrent meningitis as Ralstonia mannitolytica sp. nov. Int J Syst Evol Microbiol 51:547–558

    Article  PubMed  Google Scholar 

  • Di Domenico EG et al (2016) Development of an in vitro assay, based on the biofilm ring test®, for rapid profiling of biofilm-growing bacteria. Front Microbiol 7:1429

    Article  PubMed  PubMed Central  Google Scholar 

  • Dib J, Motok J, Zenoff VF, Ordonez O, Farias ME (2008) Occurrence of resistance to antibiotics, UV-B, and arsenic in bacteria isolated from extreme environments in high-altitude (above 4400 m) Andean wetlands. Curr Microbiol 56:510–517

    Article  CAS  PubMed  Google Scholar 

  • Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890

    Article  PubMed  PubMed Central  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estrela C, Estrela CR, Barbin EL, Spano JC, Marchesan MA, Pecora JD (2002) Mechanism of action of sodium hypochlorite. Braz Dent J 13:113–117

    Article  PubMed  Google Scholar 

  • Falcone-Dias M, Vaz-Moreira I, Manaia CM (2012) Bottled mineral water as a potential source of antibiotic resistant bacteria. Water Res 46:3612–3622

    Article  CAS  PubMed  Google Scholar 

  • Fernandez C et al (1996) Nosocomial outbreak of Burkholderia pickettii infection due to a manufactured intravenous product used in three hospitals. Clin Infect Dis 22:1092–1095

    Article  CAS  PubMed  Google Scholar 

  • Ferreira da Silva M, Vaz-Moreira I, Gonzalez-Pajuelo M, Nunes OC, Manaia CM (2007) Antimicrobial resistance patterns in Enterobacteriaceae isolated from an urban wastewater treatment plant. FEMS Microbiol Ecol 60:166–176

    Article  CAS  PubMed  Google Scholar 

  • Fiorentino A, Ferro G, Alferez MC, Polo-Lopez MI, Fernandez-Ibanez P, Rizzo L (2015) Inactivation and regrowth of multidrug resistant bacteria in urban wastewater after disinfection by solar-driven and chlorination processes. J Photochem Photobiol B 148:43–50

    Article  CAS  PubMed  Google Scholar 

  • Guttenplan SB, Kearns DB (2013) Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev 37:849–871

    Article  CAS  PubMed  Google Scholar 

  • Hijnen WA, Beerendonk EF, Medema GJ (2006) Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res 40:3–22

    Article  CAS  PubMed  Google Scholar 

  • Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005) Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171–1175

    Article  CAS  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro (ed) Mammalian protein metabolism, vol 3. Academic Press, New York

    Google Scholar 

  • Khajuria A, Praharaj AK, Grover N, Kumar M (2014) Emergence of VIM-2 metallo-beta-lactamase producing Ralstonia pickettii clinical isolate in India. Indian J Med Microbiol 32:191–193

    Article  CAS  PubMed  Google Scholar 

  • Koenig DW, Pierson DL (1997) Microbiology of the space shuttle water system. Water Sci Technol 35:59–64

    Article  CAS  PubMed  Google Scholar 

  • Kulakov LA, McAlister MB, Ogden KL, Larkin MJ, O'Hanlon JF (2002) Analysis of bacteria contaminating ultrapure water in industrial systems. Appl Environ Microbiol 68:1548–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labarca JA et al (1999) A multistate nosocomial outbreak of Ralstonia pickettii colonization associated with an intrinsically contaminated respiratory care solution. Clin Infect Dis 29:1281–1286

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindsay D, von Holy A (2006) Bacterial biofilms within the clinical setting: what healthcare professionals should know. J Hosp Infect 64:313–325

    Article  CAS  PubMed  Google Scholar 

  • Maroye P, Doermann HP, Rogues AM, Gachie JP, Megraud F (2000) Investigation of an outbreak of Ralstonia pickettii in a paediatric hospital by RAPD. J Hosp Infect 44:267–272

    Article  CAS  PubMed  Google Scholar 

  • McDonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKinney RE (1953) Staining bacterial polysaccharides. J Bacteriol 66:453

    CAS  PubMed  PubMed Central  Google Scholar 

  • McNeil MM et al (1985) Nosocomial Pseudomonas pickettii colonization associated with a contaminated respiratory therapy solution in a special care nursery. J Clin Microbiol 22:903–907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mijnendonckx K, Provoost A, Ott C, Venkateswaran K, Mahillon J, Leys N, Van Houdt R (2013) Characterization of the survival ability of Cupriavidus metallidurans and Ralstonia pickettii from space-related environments. Microb Ecol 65:347–360

    Article  CAS  PubMed  Google Scholar 

  • Moxon ER, Kroll JS (1990) The role of bacterial polysaccharide capsules as virulence factors. In: Bacterial capsules. Springer, Berlin Heidelberg, pp 65–85

  • Orme J, Rivera-Bonilla T, Loli A, Blattman NN (2015) Native valve endocarditis due to Ralstonia pickettii: a case report and literature review. Case Rep Infect Dis 2015:324675

    PubMed  PubMed Central  Google Scholar 

  • O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304

    Article  CAS  PubMed  Google Scholar 

  • Pan W, Zhao Z, Dong M (2011) Lobar pneumonia caused by Ralstonia pickettii in a sixty-five-year-old Han Chinese man: a case report. J Med Case Rep 5:377

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul D, Poddar S, Sar P (2014) Characterization of arsenite-oxidizing bacteria isolated from arsenic-contaminated groundwater of West Bengal. J Environ Sci Health A Tox Hazard Subst Environ Eng 49:1481–1492

    Article  CAS  PubMed  Google Scholar 

  • Riley PS, Weaver RE (1975) Recognition of Pseudomonas pickettii in the clinical laboratory: biochemical characterization of 62 strains. J Clin Microbiol 1:61–64

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rode TM, Langsrud S, Holck A, Moretro T (2007) Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int J Food Microbiol 116:372–383

    Article  CAS  PubMed  Google Scholar 

  • Ryan MP (2009) Genotypic and phenotypic analysis of Ralstonia pickettii high purity water isolates. University of Limerick

  • Ryan MP, Adley CC (2013) The antibiotic susceptibility of water-based bacteria Ralstonia pickettii and Ralstonia insidiosa. J Med Microbiol 62:1025–1031

    Article  CAS  PubMed  Google Scholar 

  • Ryan MP, Pembroke JT, Adley CC (2006) Ralstonia pickettii: a persistent Gram-negative nosocomial infectious organism. J Hosp Infect 62:278–284

    Article  CAS  PubMed  Google Scholar 

  • Ryan MP, Pembroke JT, Adley CC (2007) Ralstonia pickettii in environmental biotechnology: potential and applications. J Appl Microbiol 103:754–764

    Article  CAS  PubMed  Google Scholar 

  • Ryan MP, Pembroke JT, Adley CC (2009) Novel Tn4371-ICE like element in Ralstonia pickettii and genome mining for comparative elements. BMC Microbiol 9:242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan MP, Pembroke JT, Adley CC (2011) Genotypic and phenotypic diversity of Ralstonia pickettii and Ralstonia insidiosa isolates from clinical and environmental sources including high-purity water. Diversity in Ralstonia pickettii. BMC Microbiol 11:194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3:399

    Article  PubMed  PubMed Central  Google Scholar 

  • Simões LC, Simões M, Vieira MJ (2007) Biofilm interactions between distinct bacterial genera isolated from drinking water. Appl Environ Microbiol 73:6192–6200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stelzmueller I et al (2006) Ralstonia pickettii-innocent bystander or a potential threat? Clin Microbiol Infect 12:99–101

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udayappan SD et al (2017) Intestinal Ralstonia pickettii augments glucose intolerance in obesity. PLoS One 12:e0181693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaneechoutte M, De Baere T, Wauters G, Steyaert S, Claeys G, Vogelaers D, Verschraegen G (2001) One case each of recurrent meningitis and hemoperitoneum infection with Ralstonia mannitolilytica. J Clin Microbiol 39:4588–4590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaneechoutte M, Kampfer P, De Baere T, Falsen E, Verschraegen G (2004) Wautersia gen. nov., a novel genus accommodating the phylogenetic lineage including Ralstonia eutropha and related species, and proposal of Ralstonia [Pseudomonas] syzygii (Roberts et al. 1990) comb. nov. Int J Syst Evol Microbiol 54:317–327

    Article  PubMed  Google Scholar 

  • Vaz-Moreira I, Nunes OC, Manaia CM (2014) Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. FEMS Microbiol Rev 38:761–778

    Article  CAS  PubMed  Google Scholar 

  • Vaz-Moreira I, Tamames J, Martinez JL, Manaia CM (2016) Draft genome sequences of two Ralstonia pickettii strains with different aminoglycoside resistance phenotypes. Genome Announc 4:e01257–e01216

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaz-Moreira I, Nunes OC, Manaia CM (2017) Ubiquitous and persistent Proteobacteria and other Gram-negative bacteria in drinking water. Sci Total Environ 586:1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Verschraegen G, Claeys G, Meeus G, Delanghe M (1985) Pseudomonas pickettii as a cause of pseudobacteremia. J Clin Microbiol 21:278–279

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vincenti S et al (2014) Non-fermentative gram-negative bacteria in hospital tap water and water used for haemodialysis and bronchoscope flushing: prevalence and distribution of antibiotic resistant strains. Sci Total Environ 499:47–54

    Article  CAS  PubMed  Google Scholar 

  • Waugh JB, Granger WM, Gaggar A (2010) Incidence, relevance and response for Ralstonia respiratory infections. Clin Lab Sci 23:99

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao J, Allen C (2007) The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J Bacteriol 189:6415–6424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Xu YB, Xu JX, Zhang XH, Xu SH, Du QP (2015) Combined toxic effects of heavy metals and antibiotics on a Pseudomonas fluorescens strain ZY2 isolated from swine wastewater. Int J Mol Sci 16:2839–2850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by National Funds from FCT - Fundação para a Ciência e a Tecnologia through projects UID/Multi/50016/2013 and NanoDiaBac ENMed/0001/2014, and IVM grant (SFRH/BPD/87360/2012); by FCT through the project WaterJPI/0001/2013 - STARE (Stopping Antibiotic Resistance Evolution); and by Erasmus Mundus Project SUD-UE (EMA2-STRAND 1, LOT 14) through PF grant (2013-2589).

Author information

Authors and Affiliations

  1. CBQF - Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior de Biotecnologia, Universidade Católica Portuguesa, Rua Arquiteto Lobão Vital, 172, 4200-374, Porto, Portugal

    Pompeyo Ferro, Ivone Vaz-Moreira & Célia M. Manaia

Authors
  1. Pompeyo Ferro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivone Vaz-Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Célia M. Manaia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Célia M. Manaia.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferro, P., Vaz-Moreira, I. & Manaia, C.M. Association between gentamicin resistance and stress tolerance in water isolates of Ralstonia pickettii and R. mannitolilytica. Folia Microbiol 64, 63–72 (2019). https://doi.org/10.1007/s12223-018-0632-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-018-0632-1

Search

Navigation