Growth phase-dependent surface properties of Legionella pneumophila and their role in adhesion to stainless steel coated QCM-D sensors.
L. pneumophila
QCM-D
adhesion
engineered water systems
hydrophobicity
stainless steel
surface charge
Journal
Letters in applied microbiology
ISSN: 1472-765X
Titre abrégé: Lett Appl Microbiol
Pays: England
ID NLM: 8510094
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
revised:
08
04
2021
received:
30
04
2020
accepted:
17
05
2021
pubmed:
25
5
2021
medline:
6
8
2021
entrez:
24
5
2021
Statut:
ppublish
Résumé
Legionella pneumophila cell surface hydrophobicity and charge are important determinants of their mobility and persistence in engineered water systems (EWS). These surface properties may differ depending on the growth phase of L. pneumophila resulting in variable adhesion and persistence within EWS. We describe the growth-dependent variations in L. pneumophila cell surface hydrophobicity and surface charge using the microbial adhesion to hydrocarbon assay and microelectrophoresis, respectively, and their role in cell adhesion to stainless steel using a quartz crystal microbalance with dissipation (QCM-D) monitoring instrument. We observed a steady increase in L. pneumophila hydrophobicity during their lifecycle in culture media. Cell surfaces of stationary phase L. pneumophila were significantly more hydrophobic than their lag and midexponential counterparts. No significant changes in L. pneumophila cell surface charge were noted. Morphology of L. pneumophila remained relatively constant throughout their lifecycle. In the QCM-D study, lag and exponential phase L. pneumophila weakly adhered to stainless steel surfaces resulting in viscoelastic layers. In contrast, stationary phase bacteria were tightly and irreversibly bound to the surfaces, forming rigid layers. Our results suggest that the stationary phase of L. pneumophila would highly favour their adhesion to plumbing surfaces and persistence in EWS.
Substances chimiques
Stainless Steel
12597-68-1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
257-267Subventions
Organisme : Royal Society of New Zealand
ID : ESR1601
Informations de copyright
© 2021 The Society for Applied Microbiology.
Références
Allison, D.G., Evans, D.J., Brown, M.R. and Gilbert, P. (1990) Possible involvement of the division cycle in dispersal of Escherichia coli from biofilms. J Bacteriol 172, 1667-1669.
Assaidi, A., Mostafa, E., Hassan, L., Mustapha, M., Fatima, H., Mohammed, T., Zahir, H. and El Mdaghri, N. et al. (2018) Effect of temperature and plumbing materials on biofilm formation by Legionella pneumophila serogroup 1 and 2-15. J Adhes Sci Technol 32, 1471-1484.
Atlas, R.M. (1999) Legionella: from environmental habitats to disease pathology, detection and control. Environ Microbiol 1, 283-293.
Baddoo, N.R. (2008) Stainless steel in construction: a review of research, applications, challenges and opportunities. J Constr Steel Res 64, 1199-1206.
Bakterij, A.J.M.T. (2014) An overview of the influence of stainless-steel surface properties on bacterial adhesion. Mater Technol 48, 609-617.
Bohach, G.A. and Snyder, I.S. (1983) Characterisation of surfaces involved in adherence of Legionella pneumophila to Fischerella species. Infect Immun 42, 318-325.
Bohinc, K., Dražić, G., Oder, M., Jevšnik, M., Nipič, D., Godič-Torkar, K. and Raspor, P. (2014) Available surface dictates microbial adhesion capacity. Int J Adhes Adhes 50, 265-272.
Busalmen, J.P. and De Sánchez, S.R. (2001) Influence of pH and ionic strength on adhesion of a wild strain of Pseudomonas sp. to titanium. J Ind Microbiol Biotechnol 26, 303-308.
Busscher, H.J. and Weerkamp, A.H. (1987) Specific and non-specific interactions in bacterial adhesion to solid substrata. FEMS Microbiol Rev 3, 165-173.
Deepika, G., Green, R.J., Frazier, R.A. and Charalampopoulos, D. (2009) Effect of growth time on the surface and adhesion properties of Lactobacillus rhamnosus GG. J Appl Microbiol 107, 1230-1240.
Deptuła, A., Mikucka, A. and Gospodarek, E. (2004) Influence of growth conditions on cell surface hydrophobicity of multiresistant Pseudomonas aeruginosa strains. Medycyna Doświadczalna 56, 364.
Diederen, B.M.W. (2008) Legionella spp. and Legionnaires' disease. J Infect 56, 1-12.
Dixon, M.C. (2008) Quartz crystal microbalance with dissipation monitoring: enabling real-time characterisation of biological materials and their interactions. J Biomol Tech 19, 151.
Doyle, R.J. (2000) Contribution of the hydrophobic effect to microbial infection. Microbes Infect 2, 391-400.
Falkinham, J.O. (2018) Mycobacterium avium complex: adherence as a way of life. AIMS Microbiol 4, 428.
Garduno, R.A., Garduno, E., Hiltz, M. and Hoffman, P.S. (2002) Intracellular growth of Legionella pneumophila gives rise to a differentiated form dissimilar to stationary- phase forms. Infect Immun 70, 6273-6283.
Gargiulo, G., Bradford, S.A., Simunek, J., Ustohal, P., Vereecken, H. and Klumpp, E. (2008) Bacteria transport and deposition under unsaturated flow conditions: the role of water content and bacteria surface hydrophobicity. Vadose Zone J 7, 406-419.
Goulter, R.M., Gentle, I.R. and Dykes, G.A. (2009) Issues in determining factors influencing bacterial attachment: a review using the attachment of Escherichia coli to abiotic surfaces as an example. Lett Appl Microbiol 49, 1-7.
Grasso, D., Smets, B.F., Strevett, K.A., Machinist, B.D., Van Oss, C.J., Giese, R.F. and Wu, W. (1996) Impact of physiological state on surface thermodynamics and adhesion of Pseudomonas aeruginosa. Environ Sci Technol 30, 3604-3608.
Gutman, J., Walker, S.L., Freger, V. and Herzberg, M. (2013) Bacterial attachment and viscoelasticity: physicochemical and motility effects analyzed using quartz crystal microbalance with dissipation (QCM-D). Environ Sci Technol 47, 398-404.
Katsikogianni, M. and Missirlis, Y.F. (2004) Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cell Mater 8, 37-57.
Latif, U., Can, S., Hayden, O., Grillberger, P. and Dickert, F.L. (2013) Sauerbrey and anti- Sauerbrey behavioral studies in QCM sensors - detection of bioanalytes. Sens Actuators B 176, 825-830.
Liu, Y., Yang, S.F., Li, Y., Xu, H., Qin, L. and Tay, J.H. (2004) The influence of cell and substratum surface hydrophobicities on microbial attachment. J Biotechnol 110, 251-256.
Ljungh, Å. and Wadström, T. (1995) Growth conditions influence expression of cell surface hydrophobicity of staphylococci and other wound infection pathogens. Microbiol Immunol 39, 753-757.
Lorite, G.S., Rodrigues, C.M., De Souza, A.A., Kranz, C., Mizaikoff, B. and Cotta, M.A. (2011) The role of conditioning film formation and surface chemical changes on Xylella fastidiosa adhesion and biofilm evolution. J Colloid Interface Sci 359, 289-295.
Lüneberg, E., Zähringer, U., Knirel, Y.A., Steinmann, D., Hartmann, M., Steinmetz, I., Rohde, M., Köhl, J. et al. (1998) Phase-variable expression of lipopolysaccharide contributes to the virulence of Legionella pneumophila. Journal Exp Med 188, 49-60.
Marcus, I.M., Herzberg, M., Walker, S.L. and Freger, V. (2012) Pseudomonas aeruginosa attachment on QCM-D sensors: the role of cell and surface hydrophobicities. Langmuir 28, 6396-6402.
Michaud, J.M., Thompson, L.R., Kaul, D., Espinoza, J.L., Richter, R.A., Xu, Z.Z., Lee, Z., Prather, K.A., et al. (2018) Taxon-specific aerosolization of bacteria and viruses in an experimental ocean-atmosphere mesocosm. Nature Commun 9, 1-10.
Murtey, M.D. and Ramasamy, P. (2016) Sample preparations for scanning electron microscopy-life sciences. In Modern electron microscopy in physical and life sciences ed. Janecek, M. and Kral, R. pp. 161-185. London: IntechOpen.
Ngwai, Y.B. and Sabiya, G. (2007) Cultivation in different growth media affects the expression of the cell surface hydrophobicity of bacteria. Cameroon J Exp Biol 3, 26-29.
Oder, M., Kompare, B., Bohinc, K. and Torkar, K.G. (2015) The impact of material surface roughness and temperature on the adhesion of Legionella pneumophila to contact surfaces. Int J Environ Health Res 25, 469-479.
Oliva, G., Tobias, S. and Carmen, B. (2018) The life cycle of L. pneumophila: Cellular differentiation is linked to virulence and metabolism. Front Cell Infect Microbiol 8, 3.
Olofsson, A.C., Hermansson, M. and Elwing, H. (2005) Use of a quartz crystal microbalance to investigate the antiadhesive potential of N-acetyl-L-cysteine. Appl Environ Microbiol 71, 2705-2712.
Olsson, A.L.J., Mitzel, M.R. and Tufenkji, N. (2015) QCM-D for non-destructive real-time assessment of Pseudomonas aeruginosa biofilm attachment to the substratum during biofilm growth. Colloids Surf B 136, 928-934.
Pagnout, C., Jomini, S., Dadhwal, M., Caillet, C., Thomas, F. and Bauda, P. (2012) Role of electrostatic interactions in the toxicity of titanium dioxide nanoparticles toward Escherichia coli. Colloids Surf B 92, 315-321.
Percival, S.L., Beech, I.B., Edyvean, R.G.J., Knapp, J.S. and Wales, D.S. (1997) Biofilm development on 304 and 316 stainless steels in a potable water system. Water and Environ J 11, 289-294.
Percival, S.L., Knapp, J.S., Wales, D.S. and Edyvean, R.G.J. (1999) The effect of turbulent flow and surface roughness on biofilm formation in drinking water. J Ind Microbiol and Biotechnol 22, 152-159.
Phoenix, V.R., Martinez, R.E., Konhauser, K.O. and Ferris, F.G. (2002) Characterisation and implications of the cell surface reactivity of Calothrix sp. strain KC97. Appl Environ Microbiol 68, 4827-4834.
Pomorska, A., Shchukin, D., Hammond, R., Cooper, M.A., Grundmeier, G. and Johannsmann, D. (2010) Positive frequency shifts observed upon adsorbing micron-sized solid objects to a quartz crystal microbalance from the liquid phase. Anal Chem 82, 2237-2242.
Popovici, J., White, C.P., Hoelle, J., Kinkle, B.K. and Lytle, D.A. (2014) Characterisation of the cell surface properties of drinking water pathogens by microbial adhesion to hydrocarbon and electrophoretic mobility measurements. Colloids Surf B 118, 126-132.
Reichardt, K., Jacobs, E., Röske, I. and Jürgen, H.H. (2010) Legionella pneumophila carrying the virulence-associated lipopolysaccharide epitope possesses two functionally different LPS components. Microbiol 156, 2953-2961.
Rodahl, M. and Kasemo, B. (1996) A simple setup to simultaneously measure the resonant frequency and the absolute dissipation factor of a quartz crystal microbalance. Rev Sci Instrum 67, 3238-3241.
Rodgers, F.G. (1979) Ultrastructure of Legionella pneumophila. J Clin Path 32, 1195-1202.
Rosenberg, M. (2006) Microbial adhesion to hydrocarbons: twenty-five years of doing MATH. FEMS Microbiol Lett 262, 129-134.
Saini, G. (2010) Bacterial hydrophobicity: assessment techniques, applications and extension to colloids. PhD Thesis, Oregon State University, Corvallis, OR.
Saito, T., Takatsuka, T., Kato, T., Ishihara, K. and Okuda, K. (1997) Adherence of oral Streptococci to an immobilized antimicrobial agent. Arch Oral Biol 42, 539-545.
Schäfer, A., Harms, H. and Zehnder, A.J. (1998) Bacterial accumulation at the air−water interface. Environ Sci Technol 32, 3704-3712.
Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671-675.
Simoni, S.F., Harms, H., Bosma, T.N.P. and Zehnder, A.J.B. (1998) Population heterogeneity affects transport of bacteria through sand columns at low flow rates. Environ Sci Tech 32, 2100-2105.
Van Loosdrecht, M.C., Lyklema, J., Norde, W., Schraa, G. and Zehnder, A.J. (1987) Electrophoretic mobility and hydrophobicity as a measured to predict the initial steps of bacterial adhesion. Appl Environ Microbiol 53, 1898-1901.
Verdon, J., Labanowski, J., Sahr, T., Ferreira, T., Lacombe, C., Buchrieser, C., Berjeaud, J.-M. and Héchard, Y. (2011) Fatty acid composition modulates sensitivity of Legionella pneumophila to warnericin RK, an antimicrobial peptide. Biochim Biophys Acta Biomembr 1808, 1146-1153.
Walker, S.L., Hill, J.E., Redman, J.A. and Elimelech, M. (2005) Influence of growth phase on adhesion kinetics of Escherichia coli D21g. Appl Environ Microbiol 71, 3093-3099.
Wang, Y.i., Lee, S.M. and Dykes, G. (2015) The physicochemical process of bacterial attachment to abiotic surfaces: challenges for mechanistic studies, predictability and the development of control strategies. Crit Rev Microbiol 41, 452-464.
Wilson, W.W., Wade, M.M., Holman, S.C. and Champlin, F.R. (2001) Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J Microbiol Methods 43, 153-164.
Winn Jr. W.C. (2015) Legionella. Bergey's Manual of Systematics of Archaea and Bacteria 1, 44.
Young, K.D. (2006) The selective value of bacterial shape. Microbiol Mol Biol Rev 70, 660-703.
Yu, V.L., Joseph, F.P., Maddalena, C.P., Stout, J.E., Schousboe, M., Widmer, A., Summersgill, J., File, T. et al. (2002) Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired legionellosis: an international collaborative survey. J Infect Dis 186, 127-128.
Zähringer, U., Knirel, Y.A., Lindner, B., Helbig, J.H., Sonesson, A., Marre, R. and Rietschel, E.T. (1995) The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog Clin Biol Res 392, 113.
Zita, A. and Hermansson, M. (1997) Determination of bacterial cell surface hydrophobicity of single cells in cultures and in wastewater in situ. FEMS Microbiol Lett 152, 299-306.