Novel Entries in a Fungal Biofilm Matrix Encyclopedia
Abstract
Virulence of Candida is linked with its ability to form biofilms. Once established, biofilm infections are nearly impossible to eradicate. Biofilm cells live immersed in a self-produced matrix, a blend of extracellular biopolymers, many of which are uncharacterized. In this study, we provide a comprehensive analysis of the matrix manufactured by Candida albicans both in vitro and in a clinical niche animal model. We further explore the function of matrix components, including the impact on drug resistance. We uncovered components from each of the macromolecular classes (55% protein, 25% carbohydrate, 15% lipid, and 5% nucleic acid) in the C. albicans biofilm matrix. Three individual polysaccharides were identified and were suggested to interact physically. Surprisingly, a previously identified polysaccharide of functional importance, β-1,3-glucan, comprised only a small portion of the total matrix carbohydrate. Newly described, more abundant polysaccharides included β-1,2 branched β-1,6-mannans (87%) associated with unbranched β-1,6-glucans (13%) in an apparent mannan-glucan complex (MGCx). Functional matrix proteomic analysis revealed 458 distinct activities. The matrix lipids consisted of neutral glycerolipids (89.1%), polar glycerolipids (10.4%), and sphingolipids (0.5%). Examination of matrix nucleic acid identified DNA, primarily noncoding sequences. Several of the in vitro matrix components, including proteins and each of the polysaccharides, weremore »
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Medicine. Infectious Diseases
- Univ. of Wisconsin, Madison, WI (United States). National Magnetic Resonance Facility at Madison
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry
- US Dept. of Agriculture (USDA), Madison, WI (United States). Dairy Forage Research Center
- Ernst Moritz Arndt Univ., Greifswald (Germany). Universitat Inst. for Microbiology; DECODON GmbH, Greifswald (Germany). BioTechnikum
- Université du Littoral Côte d’Opale, Calais (France). Unité de Chimie Environnementale at Interactions sur le Vivant
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Univ. of Wisconsin, Madison, WI (United States). Dept. of Food Sciences
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Medicine. Infectious Diseases; Univ. of Wisconsin, Madison, WI (United States). Dept. of of Medical Microbiology and Immunology
- Carnegie Mellon Univ., Pittsburgh, PA (United States). Biological Sciences
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH); National Science Foundation (NSF)
- OSTI Identifier:
- 1626131
- Grant/Contract Number:
- R01 AI073289; P41RR005351; P41RR02301; P41GM10399; S10RR027000; DMB-8415048; OIA-9977486; BIR-9214394
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 5; Journal Issue: 4; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Zarnowski, R., Westler, W. M., Lacmbouh, G. A., Marita, J. M., Bothe, J. R., Bernhardt, J., Lounes-Hadj Sahraoui, A., Fontaine, J., Sanchez, H., Hatfield, R. D., Ntambi, J. M., Nett, J. E., Mitchell, A. P., and Andes, D. R. Novel Entries in a Fungal Biofilm Matrix Encyclopedia. United States: N. p., 2014.
Web. doi:10.1128/mbio.01333-14.
Zarnowski, R., Westler, W. M., Lacmbouh, G. A., Marita, J. M., Bothe, J. R., Bernhardt, J., Lounes-Hadj Sahraoui, A., Fontaine, J., Sanchez, H., Hatfield, R. D., Ntambi, J. M., Nett, J. E., Mitchell, A. P., & Andes, D. R. Novel Entries in a Fungal Biofilm Matrix Encyclopedia. United States. https://doi.org/10.1128/mbio.01333-14
Zarnowski, R., Westler, W. M., Lacmbouh, G. A., Marita, J. M., Bothe, J. R., Bernhardt, J., Lounes-Hadj Sahraoui, A., Fontaine, J., Sanchez, H., Hatfield, R. D., Ntambi, J. M., Nett, J. E., Mitchell, A. P., and Andes, D. R. Tue .
"Novel Entries in a Fungal Biofilm Matrix Encyclopedia". United States. https://doi.org/10.1128/mbio.01333-14. https://www.osti.gov/servlets/purl/1626131.
@article{osti_1626131,
title = {Novel Entries in a Fungal Biofilm Matrix Encyclopedia},
author = {Zarnowski, R. and Westler, W. M. and Lacmbouh, G. A. and Marita, J. M. and Bothe, J. R. and Bernhardt, J. and Lounes-Hadj Sahraoui, A. and Fontaine, J. and Sanchez, H. and Hatfield, R. D. and Ntambi, J. M. and Nett, J. E. and Mitchell, A. P. and Andes, D. R.},
abstractNote = {Virulence of Candida is linked with its ability to form biofilms. Once established, biofilm infections are nearly impossible to eradicate. Biofilm cells live immersed in a self-produced matrix, a blend of extracellular biopolymers, many of which are uncharacterized. In this study, we provide a comprehensive analysis of the matrix manufactured by Candida albicans both in vitro and in a clinical niche animal model. We further explore the function of matrix components, including the impact on drug resistance. We uncovered components from each of the macromolecular classes (55% protein, 25% carbohydrate, 15% lipid, and 5% nucleic acid) in the C. albicans biofilm matrix. Three individual polysaccharides were identified and were suggested to interact physically. Surprisingly, a previously identified polysaccharide of functional importance, β-1,3-glucan, comprised only a small portion of the total matrix carbohydrate. Newly described, more abundant polysaccharides included β-1,2 branched β-1,6-mannans (87%) associated with unbranched β-1,6-glucans (13%) in an apparent mannan-glucan complex (MGCx). Functional matrix proteomic analysis revealed 458 distinct activities. The matrix lipids consisted of neutral glycerolipids (89.1%), polar glycerolipids (10.4%), and sphingolipids (0.5%). Examination of matrix nucleic acid identified DNA, primarily noncoding sequences. Several of the in vitro matrix components, including proteins and each of the polysaccharides, were also present in the matrix of a clinically relevant in vivo biofilm. Nuclear magnetic resonance (NMR) analysis demonstrated interaction of aggregate matrix with the antifungal fluconazole, consistent with a role in drug impedance and contribution of multiple matrix components.},
doi = {10.1128/mbio.01333-14},
journal = {mBio (Online)},
number = 4,
volume = 5,
place = {United States},
year = {Tue Jul 01 00:00:00 EDT 2014},
month = {Tue Jul 01 00:00:00 EDT 2014}
}
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- Kernien, John F.; Snarr, Brendan D.; Sheppard, Donald C.
- Frontiers in Immunology, Vol. 8
The Candida albicans Biofilm Matrix: Composition, Structure and Function
journal, March 2017
- Pierce, Christopher; Vila, Taissa; Romo, Jesus
- Journal of Fungi, Vol. 3, Issue 1
The use of polyhydroxylated carboxylic acids and lactones to diminish biofilm formation of the pathogenic yeast Candida albicans
journal, January 2019
- Ishchuk, Olena P.; Sterner, Olov; Strevens, Helena
- RSC Advances, Vol. 9, Issue 19
Biofilm Exopolysaccharides of Pathogenic Fungi: Lessons from Bacteria
journal, June 2016
- Sheppard, Donald C.; Howell, P. Lynne
- Journal of Biological Chemistry, Vol. 291, Issue 24
An expanded regulatory network temporally controls C andida albicans biofilm formation
journal, April 2015
- Fox, Emily P.; Bui, Catherine K.; Nett, Jeniel E.
- Molecular Microbiology, Vol. 96, Issue 6
Portrait of Matrix Gene Expression in Candida glabrata Biofilms with Stress Induced by Different Drugs
journal, April 2018
- Rodrigues, Célia; Henriques, Mariana
- Genes, Vol. 9, Issue 4
Assessment and Optimizations of Candida albicans In Vitro Biofilm Assays
journal, May 2017
- Lohse, Matthew B.; Gulati, Megha; Valle Arevalo, Ashley
- Antimicrobial Agents and Chemotherapy, Vol. 61, Issue 5
Simple Carbohydrate Derivatives Diminish the Formation of Biofilm of the Pathogenic Yeast Candida albicans
journal, December 2019
- Ishchuk, Olena P.; Sterner, Olov; Ellervik, Ulf
- Antibiotics, Vol. 9, Issue 1
Fluconazole impacts the extracellular matrix of fluconazole-susceptible and -resistant Candida albicans and Candida glabrata biofilms
journal, January 2018
- Panariello, Beatriz Helena Dias; Klein, Marlise I.; Mima, Ewerton Garcia De Oliveira
- Journal of Oral Microbiology, Vol. 10, Issue 1
Role of Glucan-Derived Polymers in the Pathogenic Fungus Candida albicans
book, July 2019
- Prieto, Daniel; Román, Elvira; Alonso-Monge, Rebeca
- Biologically-Inspired Systems
Fungal β-1,3-Glucan Increases Ofloxacin Tolerance of Escherichia coli in a Polymicrobial E. coli/Candida albicans Biofilm
journal, March 2015
- De Brucker, Katrijn; Tan, Yulong; Vints, Katlijn
- Antimicrobial Agents and Chemotherapy, Vol. 59, Issue 6
Candida Biofilms: Threats, Challenges, and Promising Strategies
journal, February 2018
- Cavalheiro, Mafalda; Teixeira, Miguel Cacho
- Frontiers in Medicine, Vol. 5
Development and regulation of single- and multi-species Candida albicans biofilms
journal, October 2017
- Lohse, Matthew B.; Gulati, Megha; Johnson, Alexander D.
- Nature Reviews Microbiology, Vol. 16, Issue 1
The Extracellular Matrix of Candida albicans Biofilms Impairs Formation of Neutrophil Extracellular Traps
journal, September 2016
- Johnson, Chad J.; Cabezas-Olcoz, Jonathan; Kernien, John F.
- PLOS Pathogens, Vol. 12, Issue 9
Large-scale production and isolation of Candida biofilm extracellular matrix
journal, October 2016
- Zarnowski, Robert; Sanchez, Hiram; Andes, David R.
- Nature Protocols, Vol. 11, Issue 12
Pathogenesis of Candida albicans biofilm
journal, March 2016
- Tsui, Christina; Kong, Eric F.; Jabra-Rizk, Mary Ann
- Pathogens and Disease, Vol. 74, Issue 4
Divergent Approaches to Virulence in C. albicans and C. glabrata: Two Sides of the Same Coin
journal, May 2019
- Galocha, Mónica; Pais, Pedro; Cavalheiro, Mafalda
- International Journal of Molecular Sciences, Vol. 20, Issue 9
Antifungal Activity and Synergism with Azoles of Polish Propolis
preprint, May 2018
- Gucwa, Katarzyna; Kusznierewicz, Barbara; Milewski, Slawomir
Global Identification of Biofilm-Specific Proteolysis in Candida albicans
journal, November 2016
- Winter, Michael B.; Salcedo, Eugenia C.; Lohse, Matthew B.
- mBio, Vol. 7, Issue 5
Antifungal Activity and Synergism with Azoles of Polish Propolis
journal, June 2018
- Gucwa, Katarzyna; Kusznierewicz, Barbara; Milewski, Sławomir
- Pathogens, Vol. 7, Issue 2
Integration of electron microscopy and solid-state NMR analysis for new views and compositional parameters of Aspergillus fumigatus biofilms
journal, February 2019
- Reichhardt, Courtney; Joubert, Lydia-Marie; Clemons, Karl V.
- Medical Mycology, Vol. 57, Issue Supplement_2
Should the biofilm mode of life be taken into consideration for microbial biocontrol agents?
journal, February 2017
- Pandin, Caroline; Le Coq, Dominique; Canette, Alexis
- Microbial Biotechnology, Vol. 10, Issue 4
Conservation and Divergence in the Candida Species Biofilm Matrix Mannan-Glucan Complex Structure, Function, and Genetic Control
journal, April 2018
- Dominguez, Eddie; Zarnowski, Robert; Sanchez, Hiram
- mBio, Vol. 9, Issue 2
Inflammatory Cell Recruitment in Candida glabrata Biofilm Cell-Infected Mice Receiving Antifungal Chemotherapy
journal, January 2019
- Rodrigues, Célia; Correia, Alexandra; Vilanova, Manuel
- Journal of Clinical Medicine, Vol. 8, Issue 2
Community participation in biofilm matrix assembly and function
journal, March 2015
- Mitchell, Kaitlin F.; Zarnowski, Robert; Sanchez, Hiram
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 13
Special Issue: Fungal Cell Wall
journal, August 2018
- Beauvais, Anne; Latgé, Jean-Paul
- Journal of Fungi, Vol. 4, Issue 3
Microbial Biofilms in Pulmonary and Critical Care Diseases
journal, September 2016
- Boisvert, Andree-Anne; Cheng, Matthew P.; Sheppard, Don C.
- Annals of the American Thoracic Society, Vol. 13, Issue 9
Ligation of Dectin-2 with a novel microbial ligand promotes adjuvant activity for vaccination
journal, August 2017
- Wang, Huafeng; Lee, Taek-Jin; Fites, Scott J.
- PLOS Pathogens, Vol. 13, Issue 8
A conserved fungal hub protein involved in adhesion and drug resistance in the human pathogen Candida albicans
journal, December 2018
- Martin-Yken, Hélène; Bedekovic, Tina; Brand, Alexandra C.
- The Cell Surface, Vol. 4
The carboxylic acid transporters Jen1 and Jen2 affect the architecture and fluconazole susceptibility of Candida albicans biofilm in the presence of lactate
journal, November 2017
- Alves, Rosana; Mota, Sandra; Silva, Sónia
- Biofouling, Vol. 33, Issue 10
Ras signalling in pathogenic yeasts
journal, February 2018
- Pentland, Daniel R.; Piper-Brown, Elliot; Muehlschlegel, Fritz A.
- Microbial Cell, Vol. 5, Issue 2
Portrait of Matrix Gene Expression in Candida glabrata Biofilms with Stress Induced by Different Drugs
journal, April 2018
- Rodrigues, Célia; Henriques, Mariana
- Genes, Vol. 9, Issue 4
Inflammatory Cell Recruitment in Candida glabrata Biofilm Cell-Infected Mice Receiving Antifungal Chemotherapy
journal, January 2019
- Rodrigues, Célia; Correia, Alexandra; Vilanova, Manuel
- Journal of Clinical Medicine, Vol. 8, Issue 2