A Candida Biofilm-Induced Pathway for Matrix Glucan Delivery: Implications for Drug Resistance
Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes...
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| Published in | PLoS pathogens Vol. 8; no. 8; p. e1002848 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.08.2012
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1002848 |
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| Abstract | Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2, PHR1, and XOG1, respectively. We show that the enzymes are crucial for both delivery of β-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary β-1,3 glucan synthase encoded by FKS1. Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP1 matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics. |
|---|---|
| AbstractList | Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2, PHR1, and XOG1, respectively. We show that the enzymes are crucial for both delivery of β-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary β-1,3 glucan synthase encoded by FKS1. Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP1 matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics. Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2 , PHR1 , and XOG1 , respectively. We show that the enzymes are crucial for both delivery of β-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary β-1,3 glucan synthase encoded by FKS1 . Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP1 matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics. Biofilms are a community of microbes that grow attached to each other and adherent to a surface. One distinguishing feature of this form of growth is the presence of a surrounding extracellular matrix which is proposed to provide a structural scaffold and protection for biofilm cells. This later function contributes to the extreme resistance to anti-infective therapies, another innate characteristic of biofilms. One carbohydrate component of the matrix of Candida albicans , β-1, 3 glucan, has been linked to overall accumulation of matrix material and the antifungal drug resistance phenotype. Although the glucan synthase pathway has been implicated in glucan production, the delivery and incorporation of these carbohydrates into the matrix remains a mystery. The current investigation describes three gene products that serve a matrix delivery role. The functions of these gene products include glucanase and glucanosyltransferase activities. Mutants unable to produce these enzymes demonstrate reduced matrix glucan, decreased total matrix biomass accumulation, and enhanced susceptibility to antifungal drug therapy. The observations here offer insight into a novel pathway that contributes to biofilm maintenance. Enzymes in this biofilm-specific process may provide useful anti-biofilm drug targets. Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2, PHR1, and XOG1, respectively. We show that the enzymes are crucial for both delivery of β-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary β-1,3 glucan synthase encoded by FKS1. Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP1 matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics.Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2, PHR1, and XOG1, respectively. We show that the enzymes are crucial for both delivery of β-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary β-1,3 glucan synthase encoded by FKS1. Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP1 matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics. Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, β-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2, PHR1, and XOG1, respectively. We show that the enzymes are crucial for both delivery of β-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary β-1,3 glucan synthase encoded by FKS1. Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP1 matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics. Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans biofilms, [beta]-1,3 glucan, has been linked to biofilm protection from antifungal agents. In this study, we identify three glucan modification enzymes that function to deliver glucan from the cell to the extracellular matrix. These enzymes include two predicted glucan transferases and an exo-glucanase, encoded by BGL2, PHR!, and XOG1, respectively. We show that the enzymes are crucial for both delivery of [beta]-1,3 glucan to the biofilm matrix and for accumulation of mature matrix biomass. The enzymes do not appear to impact cell wall glucan content of biofilm cells, nor are they necessary for filamentation or biofilm formation. We demonstrate that mutants lacking these genes exhibit enhanced susceptibility to the commonly used antifungal, fluconazole, during biofilm growth only. Transcriptional analysis and biofilm phenotypes of strains with multiple mutations suggest that these enzymes act in a complementary fashion to distribute matrix downstream of the primary [beta]-1,3 glucan synthase encoded by FKS1. Furthermore, our observations suggest that this matrix delivery pathway works independently from the C. albicans ZAP! matrix formation regulatory pathway. These glucan modification enzymes appear to play a biofilm-specific role in mediating the delivery and organization of mature biofilm matrix. We propose that the discovery of inhibitors for these enzymes would provide promising anti-biofilm therapeutics. |
| Audience | Academic |
| Author | Ross, Kelly M. Cain, Mike T. Sanchez, Hiram Zarnowski, Robert Hamaker, Jessica Mitchell, Aaron P. Nett, Jeniel E. Taff, Heather T. Andes, David R. |
| AuthorAffiliation | 2 Department of Microbiology, Columbia University, New York, New York 1 Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, Wisconsin 3 Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania Washington University School of Medicine, United States of America |
| AuthorAffiliation_xml | – name: Washington University School of Medicine, United States of America – name: 2 Department of Microbiology, Columbia University, New York, New York – name: 3 Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania – name: 1 Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, Wisconsin |
| Author_xml | – sequence: 1 givenname: Heather T. surname: Taff fullname: Taff, Heather T. – sequence: 2 givenname: Jeniel E. surname: Nett fullname: Nett, Jeniel E. – sequence: 3 givenname: Robert surname: Zarnowski fullname: Zarnowski, Robert – sequence: 4 givenname: Kelly M. surname: Ross fullname: Ross, Kelly M. – sequence: 5 givenname: Hiram surname: Sanchez fullname: Sanchez, Hiram – sequence: 6 givenname: Mike T. surname: Cain fullname: Cain, Mike T. – sequence: 7 givenname: Jessica surname: Hamaker fullname: Hamaker, Jessica – sequence: 8 givenname: Aaron P. surname: Mitchell fullname: Mitchell, Aaron P. – sequence: 9 givenname: David R. surname: Andes fullname: Andes, David R. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22876186$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2012 Public Library of Science Taff et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, et al. (2012) A Candida Biofilm-Induced Pathway for Matrix Glucan Delivery: Implications for Drug Resistance. PLoS Pathog 8(8): e1002848. doi:10.1371/journal.ppat.1002848 2012 Taff et al 2012 Taff et al |
| Copyright_xml | – notice: COPYRIGHT 2012 Public Library of Science – notice: Taff et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, et al. (2012) A Candida Biofilm-Induced Pathway for Matrix Glucan Delivery: Implications for Drug Resistance. PLoS Pathog 8(8): e1002848. doi:10.1371/journal.ppat.1002848 – notice: 2012 Taff et al 2012 Taff et al |
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| DOI | 10.1371/journal.ppat.1002848 |
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| Keywords | Candida albicans Candidiasis Animals Biofilms Glucans Rats Fungal Proteins Glucosyltransferases Membrane Glycoproteins Mutation Drug Resistance, Fungal |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 The authors have declared that no competing interests exist. Conceived and designed the experiments: HTT JEN APM DRA. Performed the experiments: HTT JEN KMR MTC RZ HS JH APM. Contributed reagents/materials/analysis tools: HTT JEN KMR RZ HS APM DRA. Wrote the paper: HTT JEN APM DRA. |
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| Snippet | Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans... Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans... Extracellular polysaccharides are key constituents of the biofilm matrix of many microorganisms. One critical carbohydrate component of Candida albicans... |
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| SubjectTerms | Animals Antifungal agents Bacteriology Biofilms Biology Candida Candida albicans - physiology Candidiasis - genetics Candidiasis - metabolism Candidiasis - pathology Drug resistance Drug resistance in microorganisms Drug Resistance, Fungal Enzymes Fungal Proteins - genetics Fungal Proteins - metabolism Genes Glucans Glucans - genetics Glucans - metabolism Glucosyltransferases - genetics Glucosyltransferases - metabolism Health aspects Medicine Membrane Glycoproteins - genetics Membrane Glycoproteins - metabolism Microbial mats Microbiology Microorganisms Mutation Physiological aspects Rats Saccharides |
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| Title | A Candida Biofilm-Induced Pathway for Matrix Glucan Delivery: Implications for Drug Resistance |
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