Nanoscale Phenotypic Textures of Yersinia pestis Across Environmentally-Relevant Matrices
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals and Instruments
2.2. Fabrication of 3D Printed Cell-Culture Chamber
2.3. Cell Culture
2.4. Chamber-Grown Bacteria
2.5. Culturing in SESOM Medium
2.6. Chamber Experiment with Soil
2.7. Imaging and Atomic Force Microscopy
2.8. Fatty Acid Profiling
3. Results and Discussion
3.1. Chamber Design and Cell Culture
3.2. AFM Imaging of Single Y. pestis Cells
3.3. Cell Surface Hydrophobicity Using Force Spectroscopy
3.4. Whole Cell Fatty Acid Profiles
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Nicoletti, P. The epidemiology of bovine brucellosis. Adv. Vet. Sci. Comp. Med. 1980, 24, 69. [Google Scholar]
- Franz, D.R.; Jahrling, P.B.; McClain, D.J.; Hoover, D.L.; Byrne, W.R.; Pavlin, J.A.; Christopher, G.W.; Cieslak, T.J.; Friedlander, A.M.; Eitzen, E.M., Jr. Clinical recognition and management of patients exposed to biological warfare agents. Clin. Lab. Med. 2001, 21, 435–474. [Google Scholar] [CrossRef]
- Lorch, J.M.; Muller, L.K.; Russell, R.E.; O’Connor, M.; Lindner, D.L.; Blehert, D.S. Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. Appl. Environ. Microbiol. 2013, 79, 1293–1301. [Google Scholar] [CrossRef] [Green Version]
- Larsen, E.; Smith, J.J.; Norton, R.; Corkeron, M. Survival, sublethal injury, and recovery of environmental Burkholderia pseudomallei in soil subjected to desiccation. Appl. Environ. Microbiol. 2013, 79, 2424–2427. [Google Scholar] [CrossRef] [Green Version]
- Eisen, R.J.; Petersen, J.M.; Higgins, C.L.; Wong, D.; Levy, C.E.; Mead, P.S.; Schriefer, M.E.; Griffith, K.S.; Gage, K.L.; Beard, C.B. Persistence of Yersinia pestis in soil under natural conditions. Emerg. Infect. Dis. 2008, 14, 941–943. [Google Scholar] [CrossRef]
- Andrianaivoarimanana, V.; Kreppel, K.; Elissa, N.; Duplantier, J.-M.; Carniel, E.; Rajerison, M.; Jambou, R. Understanding the persistence of plague foci in Madagascar. Plos Negl. Trop. Dis. 2013, 7, e2382. [Google Scholar] [CrossRef] [Green Version]
- Ayyadurai, S.; Houhamdi, L.; Lepidi, H.; Nappez, C.; Raoult, D.; Drancourt, M. Long-term persistence of virulent Yersinia pestis in soil. Microbiology 2008, 154, 2865–2871. [Google Scholar] [CrossRef] [Green Version]
- Karimi, Y. Natural preservation of plague in soil. Bull. De La Soc. De Pathol. Exot. Et De Ses Fil. 1963, 56, 1183–1186. [Google Scholar]
- Chen, Y.-S.; Shieh, W.-J.; Goldsmith, C.S.; Metcalfe, M.G.; Greer, P.W.; Zaki, S.R.; Chang, H.-H.; Chan, H.; Chen, Y.-L. Alteration of the phenotypic and pathogenic patterns of Burkholderia pseudomallei that persist in a soil environment. Am. J. Trop. Med. Hyg. 2014, 90, 469–479. [Google Scholar] [CrossRef] [Green Version]
- NandaKafle, G.; Christie, A.A.; Vilain, S.; Brözel, V.S. Growth and extended survival of Escherichia coli O157: H7 in soil organic matter. Front. Microbiol. 2018, 9, 762. [Google Scholar] [CrossRef] [Green Version]
- Vilain, S.; Luo, Y.; Hildreth, M.B.; Brozel, V.S. Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl. Environ. Microbiol. 2006, 72, 4970–4977. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Li, J.; Feng, L.; Cao, H.; Cui, Z. An improved method for extracting bacteria from soil for high molecular weight DNA recovery and BAC library construction. J. Microbiol. 2010, 48, 728–733. [Google Scholar] [CrossRef]
- Sinclair, R.; Boone, S.A.; Greenberg, D.; Keim, P.; Gerba, C.P. Persistence of category A select agents in the environment. Appl. Environ. Microbiol. 2008, 74, 555–563. [Google Scholar] [CrossRef] [Green Version]
- Kaeberlein, T.; Lewis, K.; Epstein, S.S. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 2002, 296, 1127–1129. [Google Scholar] [CrossRef] [Green Version]
- Berdy, B.; Spoering, A.L.; Ling, L.L.; Epstein, S.S. In situ cultivation of previously uncultivable microorganisms using the ichip. Nat. Protoc. 2017, 12, 2232. [Google Scholar] [CrossRef]
- Ingham, C.J.; Sprenkels, A.; Bomer, J.; Molenaar, D.; van den Berg, A.; van Hylckama Vlieg, J.E.; de Vos, W.M. The micro-Petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc. Natl. Acad. Sci. USA 2007, 104, 18217–18222. [Google Scholar] [CrossRef] [Green Version]
- Nichols, D.; Cahoon, N.; Trakhtenberg, E.; Pham, L.; Mehta, A.; Belanger, A.; Kanigan, T.; Lewis, K.; Epstein, S. Use of ichip for high-throughput in situ cultivation of “uncultivable” microbial species. Appl. Environ. Microbiol. 2010, 76, 2445–2450. [Google Scholar] [CrossRef] [Green Version]
- Chen, T.; Elberg, S.S. Scanning electron microscopic study of virulent Yersinia pestis and Yersinia pseudotuberculosis type 1. Infect. Immun. 1977, 15, 972–977. [Google Scholar] [CrossRef] [Green Version]
- Pawlowski, D.R.; Metzger, D.J.; Raslawsky, A.; Howlett, A.; Siebert, G.; Karalus, R.J.; Garrett, S.; Whitehouse, C.A. Entry of Yersinia pestis into the viable but nonculturable state in a low-temperature tap water microcosm. PLoS ONE 2011, 6, e17585. [Google Scholar] [CrossRef]
- Day, A.P.; Oliver, J.D. Changes in membrane fatty acid composition during entry of Vibrio vulnificus into the viable but nonculturable state. J. Microbiol. 2004, 42, 69–73. [Google Scholar]
- Su, X.; Sun, F.; Wang, Y.; Hashmi, M.Z.; Guo, L.; Ding, L.; Shen, C. Identification, characterization and molecular analysis of the viable but nonculturable Rhodococcus biphenylivorans. Sci. Rep. 2015, 5, 18590. [Google Scholar] [CrossRef]
- Wilson, L.; Iqbal, K.M.; Simmons-Ehrhardt, T.; Bertino, M.F.; Shah, M.R.; Yadavalli, V.K.; Ehrhardt, C.J. Customizable 3D printed diffusion chambers for studies of bacterial pathogen phenotypes in complex environments. J. Microbiol. Methods 2019, 162, 8–15. [Google Scholar] [CrossRef]
- Wang, C.; Stanciu, C.E.; Ehrhardt, C.J.; Yadavalli, V.K. Evaluation of whole cell fixation methods for the analysis of nanoscale surface features of Yersinia pestis KIM. J. Microsc. 2016, 263, 260–267. [Google Scholar] [CrossRef]
- Schumacher, B.A. Methods for the Determination of Total Organic Carbon (TOC) in Soils and Sediments. Ph.D. Thesis, United States Environmental Protection Agency Environmental Sciences Division National Exposure Research Laboratory, Las Vegas, NV, USA, 2002. [Google Scholar]
- Kurland, N.E.; Drira, Z.; Yadavalli, V.K. Measurement of nanomechanical properties of biomolecules using atomic force microscopy. Micron 2012, 43, 116–128. [Google Scholar] [CrossRef]
- Ben-Dov, E.; Kramarsky-Winter, E.; Kushmaro, A. An in situ method for cultivating microorganisms using a double encapsulation technique. FEMS Microbiol. Ecol. 2009, 68, 363–371. [Google Scholar] [CrossRef] [Green Version]
- Aoi, Y.; Kinoshita, T.; Hata, T.; Ohta, H.; Obokata, H.; Tsuneda, S. Hollow-fiber membrane chamber as a device for in situ environmental cultivation. Appl. Environ. Microbiol. 2009, 75, 3826–3833. [Google Scholar] [CrossRef] [Green Version]
- Kienberger, F.; Ebner, A.; Gruber, H.J.; Hinterdorfer, P. Molecular recognition imaging and force spectroscopy of single biomolecules. Acc. Chem. Res. 2006, 39, 29–36. [Google Scholar] [CrossRef]
- Takahashi, H.; Shahin, V.; Henderson, R.M.; Takeyasu, K.; Edwardson, J.M. Interaction of synaptotagmin with lipid bilayers, analyzed by single-molecule force spectroscopy. Biophys. J. 2010, 99, 2550–2558. [Google Scholar] [CrossRef] [Green Version]
- Steffens, C.; Leite, F.L.; Bueno, C.C.; Manzoli, A.; Herrmann, P.S.D.P. Atomic force microscopy as a tool applied to nano/biosensors. Sensors 2012, 12, 8278–8300. [Google Scholar] [CrossRef]
- Krasikova, I.; Bakholdina, S.; Solov’eva, T. Glucose as a growth medium factor regulating lipid composition of Yersinia pseudotuberculosis. Biochemistry 2001, 66, 913–917. [Google Scholar]
- Jarrett, C.O.; Deak, E.; Isherwood, K.E.; Oyston, P.C.; Fischer, E.R.; Whitney, A.R.; Kobayashi, S.D.; DeLeo, F.R.; Hinnebusch, B.J. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Infect. Dis. 2004, 190, 782–792. [Google Scholar]
- Wang, C.; Stanciu, C.E.; Ehrhardt, C.J.; Yadavalli, V.K. The effect of growth temperature on the nanoscale biochemical surface properties of Yersinia pestis. Anal. Bioanal. Chem. 2016, 408, 5585–5591. [Google Scholar] [CrossRef] [PubMed]
- Roszak, D.; Colwell, R. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 1987, 51, 365. [Google Scholar] [CrossRef]
- Portillo, M.C.; Leff, J.W.; Lauber, C.L.; Fierer, N. Cell size distributions of soil bacterial and archaeal taxa. Appl. Environ. Microbiol. 2013, 79, 7610–7617. [Google Scholar] [CrossRef] [Green Version]
- Bakken, L.R.; Olsen, R.A. The relationship between cell size and viability of soil bacteria. Microb. Ecol. 1987, 13, 103–114. [Google Scholar] [CrossRef]
- Kjelleberg, S.; Hermansson, M. Starvation-induced effects on bacterial surface characteristics. Appl. Environ. Microbiol. 1984, 48, 497–503. [Google Scholar] [CrossRef] [Green Version]
- Van Loosdrecht, M.; Lyklema, J.; Norde, W.; Schraa, G.; Zehnder, A. The role of bacterial cell wall hydrophobicity in adhesion. Appl. Environ. Microbiol. 1987, 53, 1893–1897. [Google Scholar] [CrossRef] [Green Version]
- Van Loosdrecht, M.; Lyklema, J.; Norde, W.; Schraa, G.; Zehnder, A. Electrophoretic mobility and hydrophobicity as a measured to predict the initial steps of bacterial adhesion. Appl. Environ. Microbiol. 1987, 53, 1898–1901. [Google Scholar] [CrossRef] [Green Version]
- Zita, A.; Hermansson, M. Determination of bacterial cell surface hydrophobicity of single cells in cultures and in wastewater in situ. FEMS Microbiol. Lett. 1997, 152, 299–306. [Google Scholar] [CrossRef]
- Briandet, R.; Meylheuc, T.; Maher, C.; Bellon-Fontaine, M.N. Listeria monocytogenes Scott A: Cell surface charge, hydrophobicity, and electron donor and acceptor characteristics under different environmental growth conditions. Appl. Environ. Microbiol. 1999, 65, 5328–5333. [Google Scholar] [CrossRef] [Green Version]
- Das, S.; Kapoor, K. Effect of growth medium on hydrophobicity of Staphylococcus epidermidis. Indian J. Med. Res. 2004, 119, 107–109. [Google Scholar]
- Vadillo-Rodríguez, V.; Busscher, H.J.; Norde, W.; De Vries, J.; Van Der Mei, H.C. Dynamic cell surface hydrophobicity of Lactobacillus strains with and without surface layer proteins. J. Bacteriol. 2004, 186, 6647–6650. [Google Scholar] [CrossRef] [Green Version]
- Alsteens, D.; Dague, E.; Rouxhet, P.G.; Baulard, A.R.; Dufrêne, Y.F. Direct measurement of hydrophobic forces on cell surfaces using AFM. Langmuir 2007, 23, 11977–11979. [Google Scholar] [CrossRef]
- Hamadi, F.; Latrache, H.; Zahir, H.; Elghmari, A.; Timinouni, M.; Ellouali, M. The relation between Escherichia coli surface functional groups’ composition and their physicochemical properties. Braz. J. Microbiol. 2008, 39, 10–15. [Google Scholar] [CrossRef] [Green Version]
- Gogra, A.B.; Yao, J.; Sandy, E.H.; Zheng, S.; Zaray, G.; Koroma, B.M.; Hui, Z. Cell surface hydrophobicity (CSH) of Escherichia coli, Staphylococcus aureus and Aspergillus niger and the biodegradation of diethyl phthalate (DEP) via microcalorimetry. J. Am. Sci. 2010, 6, 78–88. [Google Scholar]
- Di Ciccio, P.; Vergara, A.; Festino, A.; Paludi, D.; Zanardi, E.; Ghidini, S.; Ianieri, A. Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control. 2015, 50, 930–936. [Google Scholar] [CrossRef]
- Yuan, Y.; Hays, M.P.; Hardwidge, P.R.; Kim, J. Surface characteristics influencing bacterial adhesion to polymeric substrates. RSC Adv. 2017, 7, 14254–14261. [Google Scholar] [CrossRef] [Green Version]
- Müller, D.J.; Dufrêne, Y.F. Atomic force microscopy: A nanoscopic window on the cell surface. Trends Cell Biol. 2011, 21, 461–469. [Google Scholar] [CrossRef]
- De Pablo, P.; Colchero, J.; Gomez-Herrero, J.; Baro, A.; Schaefer, D.; Howell, S.; Walsh, B.; Reifenberger, R. Adhesion maps using scanning force microscopy techniques. J. Adhes. 1999, 71, 339–356. [Google Scholar] [CrossRef]
- Lamprou, D.A.; Smith, J.R.; Nevell, T.G.; Barbu, E.; Willis, C.R.; Tsibouklis, J. Self-assembled structures of alkanethiols on gold-coated cantilever tips and substrates for atomic force microscopy: Molecular organisation and conditions for reproducible deposition. Appl. Surf. Sci. 2010, 256, 1961–1968. [Google Scholar] [CrossRef] [Green Version]
- Smith, T. The hydrophilic nature of a clean gold surface. J. Colloid Interface Sci. 1980, 75, 51–55. [Google Scholar] [CrossRef]
- Ma, C.D.; Acevedo-Vélez, C.; Wang, C.; Gellman, S.H.; Abbott, N.L. Interaction of the hydrophobic tip of an atomic force microscope with oligopeptides immobilized using short and long tethers. Langmuir 2016, 32, 2985–2995. [Google Scholar] [CrossRef]
- Wang, Z.; Wang, J.; Ren, G.; Li, Y.; Wang, X. Influence of core oligosaccharide of lipopolysaccharide to outer membrane behavior of Escherichia coli. Mar. Drugs 2015, 13, 3325–3339. [Google Scholar] [CrossRef] [Green Version]
- Knirel, Y.; Anisimov, A. Lipopolysaccharide of Yersinia pestis, the cause of plague: Structure, genetics, biological properties. Acta Nat. 2012, 4, 46–58. [Google Scholar] [CrossRef] [Green Version]
- Clowers, B.H.; Wunschel, D.S.; Kreuzer, H.W.; Engelmann, H.E.; Valentine, N.; Wahl, K.L. Characterization of residual medium peptides from Yersinia pestis cultures. Anal. Chem. 2013, 85, 3933–3939. [Google Scholar] [CrossRef]
- Wolska, K.; Pogorzelska, S.; Fijoł, E.; Jakubczak, A.; Bukowski, K. The effect of culture conditions on hydrophobic properties of Pseudomonas aeruginosa. Med. Dosw. I Mikrobiol. 2002, 54, 61–66. [Google Scholar]
- Kot, A.; Oszajca, A.; Jakubczak, A.; Bukowski, K.; Woźniak-Kosek, A. Evaluation of the hydrophobic properties of Yersinia enterocolitica strains isolated from humans and pigs. Med. Doświadczalna 2001, 53, 37. [Google Scholar]
- Bajerski, F.; Wagner, D.; Mangelsdorf, K. Cell membrane fatty acid composition of Chryseobacterium frigidisoli PB4T, isolated from Antarctic glacier forefield soils, in response to changing temperature and pH conditions. Front. Microbiol. 2017, 8, 677. [Google Scholar] [CrossRef]
- Denich, T.; Beaudette, L.; Lee, H.; Trevors, J. Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J. Microbiol. Methods 2003, 52, 149–182. [Google Scholar] [CrossRef]
- Leclercq, A.; Guiyoule, A.; El Lioui, M.; Carniel, E.; Decallonne, J. High Homogeneity of the Yersinia pestis Fatty Acid Composition. J. Clin. Microbiol. 2000, 38, 1545–1551. [Google Scholar] [CrossRef] [Green Version]
- Kawahara, K.; Tsukano, H.; Watanabe, H.; Lindner, B.; Matsuura, M. Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 2002, 70, 4092–4098. [Google Scholar] [CrossRef] [Green Version]
- Gianotti, A.; Iucci, L.; Guerzoni, M.E.; Lanciotti, R. Effect of acidic conditions on fatty acid composition and membrane fluidity of Escherichia coli strains isolated from Crescenza cheese. Ann. Microbiol. 2009, 59, 603. [Google Scholar] [CrossRef]
- Bodnaruk, P.; Golden, D. Influence of pH and incubation temperature on fatty acid composition and virulence factors of Yersinia enterocolitica. Food Microbiol. 1996, 13, 17–22. [Google Scholar] [CrossRef]
- Suutari, M.; Laakso, S. Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 1994, 20, 285–328. [Google Scholar] [CrossRef]
- Grogan, D.W.; Cronan, J.E. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 1997, 61, 429–441. [Google Scholar] [CrossRef]
Bacteria | Media | Technique | Comments | Ref |
---|---|---|---|---|
Pseudomonas sp., arthrobacter sp., A. globiformis, E. coli. | Mineral salt medium. Acetate, ethanol, mannitol, glucose and a-xylene as growth substrate | Water contact angle | Investigated the influence of substrate and growth conditions on hydrophobicity and electrophoretic mobility | [39] |
E. coli, P. putida, F. breve, S. marcescens, A. calcoaceticus | LB | BATH, MAC, HIC | Determined the cell surface properties directly in waste water. | [40] |
L. monocytogenes | TSYE and BHI | MATS | Hydrophobicity trend was TSYE > BHI | [41] |
S. epidermidis | HBA, BHIA, BHIB, TSB and PPB | HAA | Hydrophobicity trend was HBA> BHIA > BHIB> TSB> PPB | [42] |
Lactobacillus sp., | De Man-Rogosa-Sharpe medium | Water contact angle, force spectroscopy | Determined the changes in cell surface hydrophobicity in response to ionic strength | [43] |
Mycobacterium bovis | Sauton medium | Chemical force microscopy | Measured hydrophobic forces on cell surface | [44] |
E. coli | LLB and SLB | Water contact angle | Characterized hydrophobic and hydrophilic parts of cell surface | [45] |
E. coli, S. aureus, A. niger | LB and PSM | MATH | Determined DEP degradation using hydrophobicity. | [46] |
S. aureus | TSB | MATH | Determined cell surface hydrophobicity increase with temperature. | [47] |
E. coli | LB | Water contact angle | Determined the level of bacterial adhesion with hydrophobicity | [48] |
14:0 3-OH | 16:1 ω7c | 16:0 | 17:0 Cyclo | 18:1 ω7c | 19:0 Cyclo | |
---|---|---|---|---|---|---|
TSA-no soil | 1.3 ± 0.9 | 6.7 ± 4.4 | 39.0 ± 3.0 | 41.7 ± 4.7 | 5.2 ± 2.8 | 3.6 ± 1.0 |
TSA-soil | 1.9 ± 1.5 | 8.1 ± 3.5 | 36.9 ± 1.7 | 41.0 ± 3.9 | 6.1 ± 2.4 | 3.9 ± 1.5 |
Agar-no soil | 1.7 ± 0.2 | 3.4 ± 1.1 | 36.1 ± 0.6 | 45.7 ± 1.3 | 3.4 ± 1.6 | 7.4 ± 1.2 |
Agar-soil | 1.5 ± 0.1 | 5.2 ± 2.0 | 34.8 ± 1.7 | 43.0 ± 2.3 | 5.7 ± 1.7 | 6.4 ± 0.6 |
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Iqbal, K.M.; Bertino, M.F.; Shah, M.R.; Ehrhardt, C.J.; Yadavalli, V.K. Nanoscale Phenotypic Textures of Yersinia pestis Across Environmentally-Relevant Matrices. Microorganisms 2020, 8, 160. https://doi.org/10.3390/microorganisms8020160
Iqbal KM, Bertino MF, Shah MR, Ehrhardt CJ, Yadavalli VK. Nanoscale Phenotypic Textures of Yersinia pestis Across Environmentally-Relevant Matrices. Microorganisms. 2020; 8(2):160. https://doi.org/10.3390/microorganisms8020160
Chicago/Turabian StyleIqbal, Kanwal M., Massimo F. Bertino, Muhammed R. Shah, Christopher J. Ehrhardt, and Vamsi K. Yadavalli. 2020. "Nanoscale Phenotypic Textures of Yersinia pestis Across Environmentally-Relevant Matrices" Microorganisms 8, no. 2: 160. https://doi.org/10.3390/microorganisms8020160
APA StyleIqbal, K. M., Bertino, M. F., Shah, M. R., Ehrhardt, C. J., & Yadavalli, V. K. (2020). Nanoscale Phenotypic Textures of Yersinia pestis Across Environmentally-Relevant Matrices. Microorganisms, 8(2), 160. https://doi.org/10.3390/microorganisms8020160