Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species
Abstract
The objective of this study was to evaluate the effect of the bacterial endotoxin LPS on Candida biofilm formation in vitro. The effect of the LPS of Pseudomonas aeruginosa, Klebsiella pneumoniae, Serratia marcescens and Salmonella typhimurium on six different species of Candida, comprising Candida albicans ATCC 90028, Candida glabrata ATCC 90030, Candida krusei ATCC 6258, Candida tropicalis ATCC 13803, Candida parapsilosis ATCC 22019 and Candida dubliniensis MYA 646, was studied using a standard biofilm assay. The metabolic activity of in vitro Candida biofilms treated with LPS at 90 min, 24 h and 48 h was quantified by XTT reduction assay. Viable biofilm-forming cells were qualitatively analysed using confocal laser scanning microscopy (CLSM), while scanning electron microscopy (SEM) was employed to visualize the biofilm structure. Initially, adhesion of C. albicans was significantly stimulated by Pseudomonas and Klebsiella LPS. A significant inhibition of Candida adhesion was noted for the following combinations: C. glabrata with Pseudomonas LPS, C. tropicalis with Serratia LPS, and C. glabrata, C. parapsilosis or C. dubliniensis with Salmonella LPS (P<0.05). After 24 h of incubation, a significant stimulation of initial colonization was noted for the following combinations: C. albicans/C. glabrata with Klebsiella LPS, C. glabrata/C. tropicalis/C. krusei with Salmonella LPS. In contrast, a significant inhibition of biofilm formation was observed in C. glabrata/C. dubliniensis/C. krusei with Pseudomonas LPS, C. krusei with Serratia LPS, C. dubliniensis with Klebsiella LPS and C. parapsilosis/C. dubliniensis /C. krusei with Salmonella LPS (P<0.05). On further incubation for 48 h, a significant enhancement of biofilm maturation was noted for the following combinations: C. glabrata/C. tropicalis with Serratia LPS, C. dubliniensis with Klebsiella LPS and C. glabrata with Salmonella LPS, and a significant retardation was noted for C. parapsilosis/C. dubliniensis/C. krusei with Pseudomonas LPS, C. tropicalis with Serratia LPS, C. glabrata/C. parapsilosis/C. dubliniensis with Klebsiella LPS and C. dubliniensis with Salmonella LPS (P<0.05). These findings were confirmed by SEM and CLSM analyses. In general, the inhibition of the biofilm development of LPS-treated Candida spp. was accompanied by a scanty architecture with a reduced numbers of cells compared with the profuse and densely colonized control biofilms. These data are indicative that bacterial LPSs modulate in vitro Candida biofilm formation in a species-specific and time-dependent manner. The clinical and the biological relevance of these findings have yet to be explored.
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Biofilms persist due to their physical presence and population density, affording an almost inducible resistant phenotype despite distinct genetic alterations.
“It is known that planktonic cells generally rely on irreversible genetic changes to maintain a resistant phenotype, while biofilms are able to persist due to their physical presence and the density of the population, which affords an almost inducible resistant phenotype notwithstanding of distinct genetic alterations [130,157].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [157]
Planktonic cells generally rely on irreversible genetic changes to maintain a resistant phenotype.
“It is known that planktonic cells generally rely on irreversible genetic changes to maintain a resistant phenotype, while biofilms are able to persist due to their physical presence and the density of the population, which affords an almost inducible resistant phenotype notwithstanding of distinct genetic alterations [130,157].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [157]
Cites
Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H., Wenzel, R. P., & Edmond, M. B. (2004) · Clinical Infectious Diseases · doi:10.1086/421946 · Cited by 4,496 · see citing works
Mechanisms of biofilm resistance to antimicrobial agents
Mah, T.-F. C., & O'Toole, G. A. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01913-2 · Cited by 3,921 · see citing works
Biofilm formation as microbial development
O'Toole, G., Kaplan, H. B., & Kolter, R. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.49 · Cited by 3,571 · see citing works
Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia
Tracey, K. J., Fong, Y., Hesse, D. G., Manogue, K. R., Lee, A. T., Kuo, G. C., Lowry, S. F., & Cerami, A. (1987) · Nature · doi:10.1038/330662a0 · Cited by 2,448 · see citing works
Nosocomial infections in medical intensive care units in the United States
Richards, M. J., Edwards, J. R., Culver, D. H., & Gaynes, R. P. (1999) · Critical Care Medicine · doi:10.1097/00003246-199905000-00020 · Cited by 1,561 · see citing works
Principles and Practice of Infectious Diseases
Tigertt, W. D. (1986) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1986.35.3.tm0350030671b · Cited by 1,464 · see citing works
ENDOTOXINS AND DISEASE MECHANISMS
Morrison, D. C., & Ryan, J. L. (1987) · Annual Review of Medicine · doi:10.1146/annurev.me.38.020187.002221 · Cited by 1,111 · see citing works
Pappas, P. G., Rex, J. H., Lee, J., Hamill, R. J., Larsen, R. A., Powderly, W. G., Kauffman, C. A., Hyslop, N., Mangino, J. E., Chapman, S. W., et al. (2003) · Clinical Infectious Diseases · doi:10.1086/376906 · Cited by 832 · see citing works
Nosocomial Candidiasis: Emerging Species, Reservoirs, and Modes of Transmission
Pfaller, M. A. (1996) · Clinical Infectious Diseases · doi:10.1093/clinids/22.supplement_2.s89 · Cited by 499 · see citing works
Rangel‐Frausto, M. S., Wiblin, T., Blumberg, H. M., Saiman, L., Patterson, J., Rinaldi, M., Pfaller, M., Edwards, Jr., Jarvis, W., Dawson, J., et al. (1999) · Clinical Infectious Diseases · doi:10.1086/520194 · Cited by 430 · see citing works
Rippon, J. W. (1989) · JAMA · doi:10.1001/jama.1989.03430190139055 · Cited by 398 · see citing works
Characteristics of biofilm formation by Candida albicans.
Ramage, G., VandeWalle, K., Wickes, B. L., & Lopez-Ribot, J. L. (2001) · PubMed · Cited by 370 · see citing works
Fractions of lipopolysaccharide from Escherichia coli O111:B4 prepared by two extraction procedures.
Morrison, D., & Leive, L. (1975) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)41574-3 · Cited by 332 · see citing works
Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars
Jin, Y., Samaranayake, L. P., Samaranayake, Y. H., & Yip, H. K. (2004) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2004.04.011 · Cited by 266 · see citing works
Self-citationThe Primary Role of Lymphoreticnlar Cells in the Mediation of Host Responses to Bacterial Endotoxim
Michalek, S. M., Moore, R. N., McGhee, J. R., Rosenstreich, D. L., & Mergenhagen, S. E. (1980) · The Journal of Infectious Diseases · doi:10.1093/infdis/141.1.55 · Cited by 210 · see citing works
Morrison, D., Betz, S., & Jacobs, D. (1976) · The Journal of Experimental Medicine · doi:10.1084/jem.144.3.840 · Cited by 183 · see citing works
(2002) · ASM Press eBooks · doi:10.1128/9781555817947 · Cited by 182 · see citing works
Shifting patterns in the epidemiology of nosocomial Candida infections
Snydman, D. R. (2003) · Chest · doi:10.1378/chest.123.5_suppl.500s · Cited by 142 · see citing works
Bacterial endotoxins: chemical structure, biological activity and role in septicaemia.
Rietschel, E. T., Schade, U. F., Jensen, M., Wollenweber, H. W., Luderitz, O., & Greisman, S. G. (1982) · PubMed · Cited by 140 · see citing works
Sabra, W. A., Lünsdorf, H., & Zeng, A. (2003) · Microbiology · doi:10.1099/mic.0.26443-0 · Cited by 138 · see citing works
Critical Aggregation Concentrations of Gram-Negative Bacterial Lipopolysaccharides (LPS)
Aurell, C., & Wistrom, A. O. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9773 · Cited by 138 · see citing works
Jin, Y., Zhang, T., Samaranayake, Y. H., Fang, H. H. P., Yip, H. K., & Samaranayake, L. P. (2005) · Mycopathologia · doi:10.1007/s11046-004-6987-7 · Cited by 130 · see citing works
Self-citationPittet, D. (1995) · Archives of Internal Medicine · doi:10.1001/archinte.155.11.1177 · Cited by 115 · see citing works
Candidemia in critically ill patients: difference of outcome between medical and surgical patients
Charles, P., Doise, J. M., Quenot, J., Aube, H., Dalle, F., Chavanet, P., Milési, N., Aho, S., Portier, H., & Blettery, B. (2003) · Intensive Care Medicine · doi:10.1007/s00134-003-2002-x · Cited by 111 · see citing works
THE EPIDEMIOLOGY OF BACTERIAL SEPSIS
Rangel-Frausto, M. S. (1999) · Infectious Disease Clinics of North America · doi:10.1016/s0891-5520(05)70076-3 · Cited by 108 · see citing works
Jl, L. F. (1976) · PubMed · Cited by 90 · see citing works
Potential risk factors for infection with Candida spp. in critically ill patients
Bota, D. P., Rodriguez‐Villalobos, H., Dimopoulos, G., Mélot, C., & Vincent, J. (2004) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00873.x · Cited by 82 · see citing works
Escherichia coli and its lipopolysaccharide modulate in vitro Candida biofilm formation
Bandara, H. M. H. N., Yau, J. Y. Y., Watt, R. M., Jin, L. J., & Samaranayake, L. P. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.012989-0 · Cited by 82 · see citing works
Self-citationCandida sepsis in surgical patients
Eubanks, P. J., de Virgilio, C., Klein, S. R., & Bongard, F. S. (1993) · The American Journal of Surgery · doi:10.1016/s0002-9610(05)80666-x · Cited by 79 · see citing works
Epidemiology of Yeast Colonization in the Intensive Care Unit
Hedderwick, S. A., Lyons, M. J., Liu, M., Vázquez, J. A., & Kauffman, C. A. (2000) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s100960000348 · Cited by 79 · see citing works
Interactions between Candida Species and Bacteria in Mixed Infections
Jenkinson, H. F., & Douglas, L. (2014) · ASM Press eBooks · doi:10.1128/9781555817947.ch18 · Cited by 76 · see citing works
Palma, C., Cassone, A., Serbousek, D., Pearson, C. A., & Djeu, J. Y. (1992) · Infection and Immunity · doi:10.1128/iai.60.11.4604-4611.1992 · Cited by 62 · see citing works
Klaerner, H. G., Uknis, M. E., Acton, R. D., Dahlberg, P. S., Carlone-Jambor, C., & Dunn, D. L. (1997) · Journal of Surgical Research · doi:10.1006/jsre.1997.5110 · Cited by 60 · see citing works
Microbial biofilms: e pluribus unum
Nobile, C. J., & Mitchell, A. P. (2007) · Current Biology · doi:10.1016/j.cub.2007.02.035 · Cited by 59 · see citing works
Pseudomonas aeruginosa PAO1 ceases to express serotype-specific lipopolysaccharide at 45 degrees C
Makin, S. A., & Beveridge, T. J. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.11.3350-3352.1996 · Cited by 48 · see citing works
Luchi, M., & Morrison, D. C. (2000) · Infection and Immunity · doi:10.1128/iai.68.4.1899-1904.2000 · Cited by 46 · see citing works
Akagawa, G., Abe, S., & Yamaguchi, H. (1995) · The Journal of Infectious Diseases · doi:10.1093/infdis/171.6.1539 · Cited by 46 · see citing works
McLean, R. J. C., Bates, C. L., Barnes, M. B., et al. (2004) · doi:10.1128/9781555817718.ch20 · Cited by 37 · see citing works
Escherichia coli and TNF-α Modulate Macrophage Phagocytosis of Candida glabrata
Hess, D. J., Henry‐Stanley, M. J., Bendel, C. M., Zhang, B., Johnson, M.-A., & Wells, C. L. (2008) · Journal of Surgical Research · doi:10.1016/j.jss.2008.07.022 · Cited by 28 · see citing works
Burd, R. S., Raymond, C. S., & Dunn, D. L. (1992) · Journal of Surgical Research · doi:10.1016/0022-4804(92)90125-j · Cited by 26 · see citing works
Vukajlovich, S. W., & Morrison, D. C. (1985) · The Journal of Immunology · doi:10.4049/jimmunol.135.4.2546 · Cited by 16 · see citing works
Effect of lipopolysaccharide on virulence of intestinal candida albicans1
Henry‐Stanley, M. J., Hess, D. J., Erickson, E. A., Garni, R. M., & Wells, C. L. (2003) · Journal of Surgical Research · doi:10.1016/s0022-4804(03)00156-2 · Cited by 15 · see citing works
Structural requirements for gelation of the Limulus amebocyte lysate by endotoxin.
Dc, M., Sw, V., Jl, R., et al. (1987) · PubMed · Cited by 14 · see citing works
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Rodrigues, C. F., Silva, S., & Henriques, M. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2009-3 · Cited by 268 · see citing works
Mowat, E., Rajendran, R., Williams, C., McCulloch, E., Jones, B., Lang, S., & Ramage, G. (2010) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.02130.x · Cited by 199 · see citing works
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Rodrigues, C., Rodrigues, M., Silva, S., & Henriques, M. (2017) · Journal of Fungi · doi:10.3390/jof3010011 · Cited by 129 · see citing works
Bandara, H. M. H. N., K Cheung, B. P., Watt, R. M., Jin, L. J., & Samaranayake, L. P. (2013) · Molecular Oral Microbiology · doi:10.1111/omi.12006 · Cited by 57 · see citing works
Self-citation
- Authors
- Bandara, H. M. H. N., Lam, O. L. T., Watt, R. M., Jin, L. J., & Samaranayake, L. P.
- Affiliations
- Oral Biosciences, Faculty of Dentistry, University of Hong Kong, 5/F Prince Philip Dental Hospital, 34 Hospital Road, Sai Ying Pun, Hong Kong SAR
- University of Hong Kong (HK)
- Prince Philip Dental Hospital (CN)
- Venue
- Journal of Medical Microbiology
- Publisher
- Microbiology Society
- Published
- 2010-10-01
- Volume
- 59
- Issue
- 10
- Pages
- 1225-1234
- ISSN
- 0022-2615 (ISSN-L)
- 1473-5644
- OpenAlex
- W2134250526
- Cited by
- 68
- References
- 43
- Citations by year
- 2025: 4 · 2024: 2 · 2023: 3 · 2021: 1 · 2020: 6 · 2019: 5 · 2018: 7 · 2017: 4 · 2016: 7 · 2015: 8 · 2014: 4 · 2013: 9 · 2012: 4
- FWCI
- 3.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Medical Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (publishedVersion)
- The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
- Explore Bristol Research (submittedVersion)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- lipopolysaccharide, bacterial endotoxin, Candida albicans, Candida glabrata, Candida tropicalis, Candida parapsilosis, Candida krusei, Candida dubliniensis, Pseudomonas aeruginosa, Klebsiella pneumoniae, Serratia marcescens, Salmonella typhimurium, yeast-bacteria interactions, biofilm adhesion, biofilm maturation, biofilm inhibition
- MeSH terms
- Antibiosis, Candida, Cell Adhesion, Cell Wall, Gram-Negative Bacteria, Humans, Lipopolysaccharides, Oxidation-Reduction, Tetrazolium Salts, Time Factors, Biofilms, Microscopy, Confocal, Microbial Viability
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