Skip to main content
SpringerLink
Log in

Cells of Escherichia coli are protected against severe chemical stress by co-habiting cell aggregates formed by Pseudomonas aeruginosa

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bacterial cells within biofilms and cell aggregates show increased resistance against chemical stress compared with suspended cells. It is not known whether bacteria that co-habit biofilms formed by other bacteria also acquire such resistance. This scenario was investigated in a proof-of-principle experiment with Pseudomonas aeruginosa strain PAO1 as cell aggregate-forming bacterium and Escherichia coli strain MG1655 as potential co-habiting bacterium equipped with an inducible bioluminescence system. Cell aggregation of strain PAO1 can be induced by the toxic detergent sodium dodecyl sulfate (SDS). In single cultures of strain MG1655, bioluminescence was inhibited by the protonophor carbonylcyanide-m-chlorophenylhydrazone (CCCP) but the cells were still viable. By applying CCCP and SDS together, cells of strain MG1655 lost their bioluminescence and viability indicating the importance of energy-dependent resistance mechanisms against SDS. In co-suspensions with strain PAO1, bioluminescence of strain MG1655 was sustained in the presence of SDS and CCCP. Image analysis showed that bioluminescent cells were located in cell aggregates formed by strain PAO1. Thus, cells of strain MG1655 that co-habited cell aggregates formed by strain PAO1 were protected against a severe chemical stress that was lethal to them in single cultures. Co-habiting could lead to increased survival of pathogens in clinical settings and could be employed in biotechnological applications involving toxic milieus.

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

  • Balaban NQ, Gerdes K, Lewis K, McKinney JD (2013) A problem of persistence: still more questions than answers? Nat Rev Microbiol 11(8):587–591

    Article  CAS  PubMed  Google Scholar 

  • Beatson SA, Whitchurch CB, Semmler ABT, Mattick JS (2002) Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J Bacteriol 184(13):3598–3604

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beech IB, Sunner JA, Hiraoka K (2005) Microbe-surface interactions in biofouling and biocorrosion processes. Int Microbiol 8(3):157–168

    CAS  PubMed  Google Scholar 

  • Burmølle M, Thomsen TR, Fazli M, Dige I, Christensen L, Homøe P, Tvede M, Nyvad B, Tolker-Nielsen T, Givskov M, Moser C, Kirketerp-Møller K, Johansen HK, Høiby N, Jensen PØ, Sørensen SJ, Bjarnsholt T (2010) Biofilms in chronic infections—a matter of opportunity—monospecies biofilms in multispecies infections. FEMS Immunol Med Microbiol 59(3):324–336

    PubMed  Google Scholar 

  • Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22(2):84–91

    Article  PubMed  Google Scholar 

  • Cerqueira L, Oliveira JA, Nicolau A, Azevedo NF, Vieira MJ (2013) Biofilm formation with mixed cultures of Pseudomonas aeruginosa/Escherichia coli on silicone using artificial urine to mimic urinary catheters. Biofouling 29(7):829–840

    Article  CAS  PubMed  Google Scholar 

  • Diehl A, von Wintzingerode F, Görisch H (1998) Quinoprotein ethanol dehydrogenase of Pseudomonas aeruginosa is a homodimer–sequence of the gene and deduced structural properties of the enzyme. Eur J Biochem 257(2):409–419

    Article  CAS  PubMed  Google Scholar 

  • Edwards SJ, Kjellerup BV (2013) Applications of biofilms in bioremediation and biotransformation of persistent organic pollutants, pharmaceuticals/personal care products, and heavy metals. Appl Microbiol Biotechnol 97(23):9909–9921

    Article  CAS  PubMed  Google Scholar 

  • Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36(5):990–1004

    Article  CAS  PubMed  Google Scholar 

  • Fazli M, Almblad H, Rybtke ML, Givskov M, Eberl L, Tolker-Nielsen T (2014) Regulation of biofilm formation in Pseudomonas and Burkholderia species. Environ Microbiol 16(7):1961–1981

    Article  CAS  PubMed  Google Scholar 

  • Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13(1):34–40

    Article  CAS  PubMed  Google Scholar 

  • Helenius A, Simons K (1975) Solubilization of membranes by detergents. Biochim Biophys Acta 415(1):29–79

    Article  CAS  PubMed  Google Scholar 

  • Huang C-J, Lin H, Yang X (2012) Industrial production of recombinant therapeutics in Escherichia coli and its recent advancements. J Ind Microbiol Biotechnol 39:383–399

    Article  CAS  PubMed  Google Scholar 

  • Jagmann N, Brachvogel H-P, Philipp B (2010) Parasitic growth of Pseudomonas aeruginosa in co-culture with the chitinolytic bacterium Aeromonas hydrophila. Environ Microbiol 12(6):1787–1802

    Article  CAS  PubMed  Google Scholar 

  • Jagmann N, Philipp B (2014) Design of synthetic microbial communities for biotechnological production processes. J Biotechnol 184:209–218

    Article  CAS  PubMed  Google Scholar 

  • Katharios-Lanwermeyer S, Xi C, Jakubovics NS, Rickard AH (2014) Mini-review: microbial coaggregation: ubiquity and implications for biofilm development. Biofouling 30(10):1235–1251

    Article  CAS  PubMed  Google Scholar 

  • Klayman BJ, Volden PA, Stewart PS, Camper AK (2009) Escherichia coli O157:H7 requires colonizing partner to adhere and persist in a capillary flow cell. Environ Sci Technol 43(6):2105–2111

    Article  CAS  PubMed  Google Scholar 

  • Klebensberger J, Rui O, Fritz E, Schink B, Philipp B (2006) Cell aggregation of Pseudomonas aeruginosa strain PAO1 as an energy-dependent stress response during growth with sodium dodecyl sulfate. Arch Microbiol 185(6):417–427

    Article  CAS  PubMed  Google Scholar 

  • Klebensberger J, Lautenschlager K, Bressler D, Wingender J, Philipp B (2007) Detergent-induced cell aggregation in subpopulations of Pseudomonas aeruginosa as a preadaptive survival strategy. Environ Microbiol 9(9):2247–2259

    Article  PubMed  Google Scholar 

  • Klebensberger J, Birkenmaier A, Geffers R, Kjelleberg S, Philipp B (2009) SiaA and SiaD are essential for inducing autoaggregation as a specific response to detergent stress in Pseudomonas aeruginosa. Environ Microbiol 11(12):3073–3086

    Article  CAS  PubMed  Google Scholar 

  • Kolenbrander PE (2011) Multispecies communities: interspecies interactions influence growth on saliva as sole nutritional source. Int J Oral Sci 3(2):49–54

    Article  PubMed Central  PubMed  Google Scholar 

  • Kurvet I, Ivask A, Bondarenko O, Sihtmäe M, Kahru A (2011) LuxCDABE-transformed constitutively bioluminescent Escherichia coli for toxicity screening: comparison with naturally luminous Vibrio fischeri. Sensors 11:7865–7878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laverty G, Gorman SP, Gilmore BF (2014) Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens 3:596–632

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leimbach A, Hacker J, Dobrindt U (2013) E. coli as an all-rounder: the thin line between commensalism and pathogenicity. Curr Top Microbiol Immunol 358:3–32

    PubMed  Google Scholar 

  • Lewis K (2012) Persister cells: molecular mechanisms related to antibiotic tolerance. Handb Exp Pharmacol 211:121–133

    Article  CAS  PubMed  Google Scholar 

  • Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36(4):893–916

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Masák J, Cejková A, Schreiberová O, Rezanka T (2014) Pseudomonas biofilms: possibilities of their control. FEMS Microbiol Ecol 89(1):1–14

    Article  PubMed  Google Scholar 

  • Nikaido H, Pagès J-M (2012) Broad-specificity efflux pumps and their role in multidrug resistance of gram-negative bacteria. FEMS Microbiol Rev 36(2):340–363

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rajagopal S, Sudarsan N, Nickerson KW (2002) Sodium dodecyl sulfate hypersensitivity of clpP and clpB mutants of Escherichia coli. Appl Environ Microbiol 68(8):4117–4121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rendueles O, Ghigo J-M (2012) Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36(5):972–989

    Article  CAS  PubMed  Google Scholar 

  • Rosche B, Li XZ, Hauer B, Schmid A, Buehler K (2009) Microbial biofilms: a concept for industrial catalysis? Trends Biotechnol 27(11):636–643

    Article  CAS  PubMed  Google Scholar 

  • Scott RA, Weil J, Le PT, Williams P, Fray RG, von Bodman SB, Savka MA (2006) Long- and short-chain plant-produced bacterial N-acyl-homoserine lactones become components of phyllosphere, rhizosphere, and soil. Mol Plant Microbe Interact 19(3):227–239

    Article  CAS  PubMed  Google Scholar 

  • Serra DO, Hengge R (2014) Stress responses go three dimensional—the spatial order of physiological differentiation in bacterial macrocolony biofilms. Environ Microbiol 16(6):1455–1471

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK, Chhabra SR, Williams P, Macintyre S, Stewart GS (1997) Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 179(17):5271–5281

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thanassi DG, Cheng LW, Nikaido H (1997) Active efflux of bile salts by Escherichia coli. J Bacteriol 179(8):2512–2518

    PubMed Central  CAS  PubMed  Google Scholar 

  • Van Acker H, Van Dijck P, Coenye T (2014) Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol 22(6):326–333

    Article  PubMed  Google Scholar 

  • Van Houdt R, Michiels CW (2010) Biofilm formation and the food industry, a focus on the bacterial outer surface. J Appl Microbiol 109(4):1117–1131

    Article  PubMed  Google Scholar 

  • Wang S, Liu X, Liu H, Li Z, Guo Y, Yu S, Wozniak DJ, Ma LZ (2014) The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ Microbiol Rep. doi:10.1111/1758-2229.12252

    PubMed Central  Google Scholar 

  • Williams P, Cámara M (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12:182–191

Download references

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Author notes

  1. Sebastian Franz Henke

    Present address: Molekulare Nephrologie, Medizinische Klinik und Poliklinik D, Westfälische Wilhelms-Universität (WWU) Münster, Münster, Germany

Authors and Affiliations

  1. Institut für Molekulare Mikrobiologie und Biotechnologie, Westfälische Wilhelms-Universität (WWU) Münster, Corrensstr. 3, 48149, Münster, Germany

    Nina Jagmann, Sebastian Franz Henke & Bodo Philipp

Authors
  1. Nina Jagmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sebastian Franz Henke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bodo Philipp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bodo Philipp.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jagmann, N., Henke, S.F. & Philipp, B. Cells of Escherichia coli are protected against severe chemical stress by co-habiting cell aggregates formed by Pseudomonas aeruginosa . Appl Microbiol Biotechnol 99, 8285–8294 (2015). https://doi.org/10.1007/s00253-015-6726-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6726-7

Keywords

Search

Navigation