Abstract
A key feature of biofilms is their production of an extracellular matrix. This material covers the biofilm cells, providing a protective barrier to the surrounding environment. During an infection setting, this can include such offenses as host cells and products of the immune system as well as drugs used for treatment. Studies over the past two decades have revealed the matrix from different biofilm species to be as diverse as the microbes themselves. This chapter will review the composition and roles of matrix from fungal biofilms, with primary focus on Candida species, Saccharomyces cerevisiae, Aspergillus fumigatus, and Cryptococcus neoformans. Additional coverage will be provided on the antifungal resistance proffered by the Candida albicans matrix, which has been studied in the most depth. A brief section on the matrix produced by bacterial biofilms will be provided for comparison. Current tools for studying the matrix will also be discussed, as well as suggestions for areas of future study in this field.
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References
Al-Fattani MA, Douglas LJ (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55(Pt 8):999–1008. doi:10.1099/jmm.0.46569-0
Alvarez M, Saylor C, Casadevall A (2008) Antibody action after phagocytosis promotes Cryptococcus neoformans and Cryptococcus gattii macrophage exocytosis with biofilm-like microcolony formation. Cell Microbiol 10(8):1622–1633. doi:10.1111/j.1462-5822.2008.01152.x
Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, Pitula A (2004) Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72(10):6023–6031. doi:10.1128/iai.72.10.6023-6031.2004
Baillie GS, Douglas LJ (2000) Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J Antimicrob Chemother 46(3):397–403
Bamford NC, Snarr BD, Gravelat FN, Little DJ, Lee MJ, Zacharias CA, Chabot JC, Geller AM, Baptista SD, Baker P, Robinson H, Howell PL, Sheppard DC (2015) Sph3 is a glycoside hydrolase required for the biosynthesis of galactosaminogalactan in Aspergillus fumigatus. J Biol Chem. doi:10.1074/jbc.M115.679050
Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, Henry C, Paris S, Mallet A, Prevost MC, Latge JP (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9(6):1588–1600. doi:10.1111/j.1462-5822.2007.00895.x
Beauvais A, Loussert C, Prevost MC, Verstrepen K, Latge JP (2009) Characterization of a biofilm-like extracellular matrix in FLO1-expressing Saccharomyces cerevisiae cells. FEMS Yeast Res 9(3):411–419. doi:10.1111/j.1567-1364.2009.00482.x
Beauvais A, Fontaine T, Aimanianda V, Latge JP (2014) Aspergillus cell wall and biofilm. Mycopathologia 178(5–6):371–377. doi:10.1007/s11046-014-9766-0
Berk V, Fong JC, Dempsey GT, Develioglu ON, Zhuang X, Liphardt J, Yildiz FH, Chu S (2012) Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 337(6091):236–239. doi:10.1126/science.1222981
Bojsen RK, Andersen KS, Regenberg B (2012) Saccharomyces cerevisiae--a model to uncover molecular mechanisms for yeast biofilm biology. FEMS Immunol Med Microbiol 65(2):169–182. doi:10.1111/j.1574-695X.2012.00943.x
Branda SS, Vik S, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13(1):20–26. doi:10.1016/j.tim.2004.11.006
Bugli F, Posteraro B, Papi M, Torelli R, Maiorana A, Paroni Sterbini F, Posteraro P, Sanguinetti M, De Spirito M (2013) In vitro interaction between alginate lyase and amphotericin B against Aspergillus fumigatus biofilm determined by different methods. Antimicrob Agents Chemother 57(3):1275–1282. doi:10.1128/aac.01875-12
Cegelski L (2015) Bottom-up and top-down solid-state NMR approaches for bacterial biofilm matrix composition. J Magn Reson 253:91–97. doi:10.1016/j.jmr.2015.01.014
Chaffin WL (2008) Candida albicans cell wall proteins. Microbiol Mol Biol Rev 72(3):495–544. doi:10.1128/MMBR.00032-07
Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GC, Parsek MR (2011) The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog 7(1), e1001264. doi:10.1371/journal.ppat.1001264
Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322
de Groot PW, Klis FM (2008) The conserved PA14 domain of cell wall-associated fungal adhesins governs their glycan-binding specificity. Mol Microbiol 68(3):535–537. doi:10.1111/j.1365-2958.2008.06182.x
Donlan RM (2001) Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis Off Publ Infect Dis Soc Am 33(8):1387–1392. doi:10.1086/322972
Dranginis AM, Rauceo JM, Coronado JE, Lipke PN (2007) A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71(2):282–294. doi:10.1128/mmbr.00037-06
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith FJ (1951) A Colorimetric Method for the Determination of Sugars. Nature 168(4265):167
Elsholz AK, Wacker SA, Losick R (2014) Self-regulation of exopolysaccharide production in Bacillus subtilis by a tyrosine kinase. Genes Dev 28(15):1710–1720. doi:10.1101/gad.246397.114
Faria-Oliveira F, Carvalho J, Belmiro CL, Martinez-Gomariz M, Hernaez ML, Pavao M, Gil C, Lucas C, Ferreira C (2014) Methodologies to generate, extract, purify and fractionate yeast ECM for analytical use in proteomics and glycomics. BMC Microbiol 14:244. doi:10.1186/s12866-014-0244-0
Faria-Oliveira F, Carvalho J, Belmiro CL, Ramalho G, Pavao M, Lucas C, Ferreira C (2015) Elemental biochemical analysis of the polysaccharides in the extracellular matrix of the yeast Saccharomyces cerevisiae. J Basic Microbiol 55(6):685–694. doi:10.1002/jobm.201400781
Fernandes T, Silva S, Henriques M (2015) Candida tropicalis biofilm’s matrix-involvement on its resistance to amphotericin B. Diagn Microbiol Infect Dis. doi:10.1016/j.diagmicrobio.2015.06.015
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633. doi:10.1038/nrmicro2415
Fong JC, Syed KA, Klose KE, Yildiz FH (2010) Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology 156(Pt 9):2757–2769. doi:10.1099/mic.0.040196-0
Franklin MJ, Nivens DE, Weadge JT, Howell PL (2011) Biosynthesis of the Pseudomonas aeruginosa Extracellular Polysaccharides, Alginate, Pel, and Psl. Front Microbiol 2:167. doi:10.3389/fmicb.2011.00167
Gravelat FN, Beauvais A, Liu H, Lee MJ, Snarr BD, Chen D, Xu W, Kravtsov I, Hoareau CM, Vanier G, Urb M, Campoli P, Al Abdallah Q, Lehoux M, Chabot JC, Ouimet MC, Baptista SD, Fritz JH, Nierman WC, Latge JP, Mitchell AP, Filler SG, Fontaine T, Sheppard DC (2013) Aspergillus galactosaminogalactan mediates adherence to host constituents and conceals hyphal beta-glucan from the immune system. PLoS Pathog 9(8), e1003575. doi:10.1371/journal.ppat.1003575
Gresnigt MS, Bozza S, Becker KL, Joosten LA, Abdollahi-Roodsaz S, van der Berg WB, Dinarello CA, Netea MG, Fontaine T, De Luca A, Moretti S, Romani L, Latge JP, van de Veerdonk FL (2014) A polysaccharide virulence factor from Aspergillus fumigatus elicits anti-inflammatory effects through induction of Interleukin-1 receptor antagonist. PLoS Pathog 10(3), e1003936. doi:10.1371/journal.ppat.1003936
Guo B, Styles CA, Feng Q, Fink GR (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci U S A 97(22):12158–12163. doi:10.1073/pnas.220420397
Harriott MM, Lilly EA, Rodriguez TE, Fidel PL Jr, Noverr MC (2010) Candida albicans forms biofilms on the vaginal mucosa. Microbiology 156(Pt 12):3635–3644. doi:10.1099/mic.0.039354-0
Hawser SP, Douglas LJ (1994) Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 62(3):915–921
Hawser SP, Baillie GS, Douglas LJ (1998) Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol 47(3):253–256
Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR (2015) Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol Rev. doi:10.1093/femsre/fuv015
Hung C, Zhou Y, Pinkner JS, Dodson KW, Crowley JR, Heuser J, Chapman MR, Hadjifrangiskou M, Henderson JP, Hultgren SJ (2013) Escherichia coli biofilms have an organized and complex extracellular matrix structure. mBio 4(5):e00645-13. doi:10.1128/mBio.00645-13
Ishigami M, Nakagawa Y, Hayakawa M, Iimura Y (2004) FLO11 is essential for flor formation caused by the C-terminal deletion of NRG1 in Saccharomyces cerevisiae. FEMS Microbiol Lett 237(2):425–430. doi:10.1016/j.femsle.2004.07.012
Johnson CC, Yu A, Lee H, Fidel PL Jr, Noverr MC (2012) Development of a contemporary animal model of Candida albicans-associated denture stomatitis using a novel intraoral denture system. Infect Immun 80(5):1736–1743. doi:10.1128/iai.00019-12
Kaur S, Singh S (2014) Biofilm formation by Aspergillus fumigatus. Med Mycol Off Publ Int Soc Human Animal Mycol 52(1):2–9. doi:10.3109/13693786.2013.819592
Kuthan M, Devaux F, Janderova B, Slaninova I, Jacq C, Palkova Z (2003) Domestication of wild Saccharomyces cerevisiae is accompanied by changes in gene expression and colony morphology. Mol Microbiol 47(3):745–754
LaFleur MD, Kumamoto CA, Lewis K (2006) Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 50(11):3839–3846. doi:10.1128/AAC.00684-06
Lal P, Sharma D, Pruthi P, Pruthi V (2010) Exopolysaccharide analysis of biofilm-forming Candida albicans. J Appl Microbiol 109(1):128–136. doi:10.1111/j.1365-2672.2009.04634.x
Lattif AA, Chabot JC, Chang C, Liu S, Zhou G, Chance MR, Ghannoum MA, Mukherjee PK (2008) Proteomics and Pathway Mapping Analyses Reveal Phase-Dependent Overexpression of Proteins Associated with Carbohydrate Metabolic Pathways in Candida albicans Biofilms. Open Proteom J 1:5–26
Lee MJ, Gravelat FN, Cerone RP, Baptista SD, Campoli PV, Choe SI, Kravtsov I, Vinogradov E, Creuzenet C, Liu H, Berghuis AM, Latge JP, Filler SG, Fontaine T, Sheppard DC (2014) Overlapping and distinct roles of Aspergillus fumigatus UDP-glucose 4-epimerases in galactose metabolism and the synthesis of galactose-containing cell wall polysaccharides. J Biol Chem 289(3):1243–1256. doi:10.1074/jbc.M113.522516
Loussert C, Schmitt C, Prevost MC, Balloy V, Fadel E, Philippe B, Kauffmann-Lacroix C, Latge JP, Beauvais A (2010) In vivo biofilm composition of Aspergillus fumigatus. Cell Microbiol 12(3):405–410. doi:10.1111/j.1462-5822.2009.01409.x
Ma L, Conover M, Lu H, Parsek MR, Bayles K, Wozniak DJ (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5(3), e1000354. doi:10.1371/journal.ppat.1000354
Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36(4):893–916. doi:10.1111/j.1574-6976.2011.00322.x
Martinez LR, Casadevall A (2005) Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect Immun 73(10):6350–6362. doi:10.1128/iai.73.10.6350-6362.2005
Martinez LR, Casadevall A (2006a) Cryptococcus neoformans cells in biofilms are less susceptible than planktonic cells to antimicrobial molecules produced by the innate immune system. Infect Immun 74(11):6118–6123. doi:10.1128/iai.00995-06
Martinez LR, Casadevall A (2006b) Susceptibility of Cryptococcus neoformans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother 50(3):1021–1033. doi:10.1128/aac.50.3.1021-1033.2006
Martinez LR, Casadevall A (2007) Cryptococcus neoformans biofilm formation depends on surface support and carbon source and reduces fungal cell susceptibility to heat, cold, and UV light. Appl Environ Microbiol 73(14):4592–4601. doi:10.1128/aem.02506-06
Martinez LR, Casadevall A (2015) Biofilm Formation by Cryptococcus neoformans. Microbiol Spect 3:3. doi:10.1128/microbiolspec.MB-0006-2014
Martinez LR, Mihu MR, Han G, Frases S, Cordero RJ, Casadevall A, Friedman AJ, Friedman JM, Nosanchuk JD (2010) The use of chitosan to damage Cryptococcus neoformans biofilms. Biomaterials 31(4):669–679. doi:10.1016/j.biomaterials.2009.09.087
Martins M, Uppuluri P, Thomas DP, Cleary IA, Henriques M, Lopez-Ribot JL, Oliveira R (2010) Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia 169(5):323–331. doi:10.1007/s11046-009-9264-y
Martins M, Henriques M, Lopez-Ribot JL, Oliveira R (2012) Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses 55(1):80–85. doi:10.1111/j.1439-0507.2011.02047.x
Marvasi M, Visscher PT, Casillas Martinez L (2010) Exopolymeric substances (EPS) from Bacillus subtilis: polymers and genes encoding their synthesis. FEMS Microbiol Lett 313(1):1–9. doi:10.1111/j.1574-6968.2010.02085.x
Mitchell KF, Taff HT, Cuevas MA, Reinicke EL, Sanchez H, Andes DR (2013) Role of Matrix beta-1,3 Glucan in Antifungal Resistance of Non-albicans Candida Biofilms. Antimicrob Agents Chemother 57(4):1918–1920. doi:10.1128/AAC.02378-12
Mitchell KF, Zarnowski R, Sanchez H, Edward JA, Reinicke EL, Nett JE, Mitchell AP, Andes DR (2015) Community participation in biofilm matrix assembly and function. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1421437112
Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA (2003) Mechanism of Fluconazole Resistance in Candida albicans Biofilms: Phase-Specific Role of Efflux Pumps and Membrane Sterols. Infect Immun 71(8):4333–4340. doi:10.1128/iai.71.8.4333-4340.2003
Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4(11), e1000213. doi:10.1371/journal.ppat.1000213
Nett J, Lincoln L, Marchillo K, Andes D (2007a) Beta −1,3 glucan as a test for central venous catheter biofilm infection. J Infect Dis 195(11):1705–1712. doi:10.1086/517522
Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, VanHandel M, Andes D (2007b) Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 51(2):510–520. doi:10.1128/aac.01056-06
Nett JE, Lepak AJ, Marchillo K, Andes DR (2009) Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis 200(2):307–313. doi:10.1086/599838
Nett JE, Crawford K, Marchillo K, Andes DR (2010a) Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother 54(8):3505–3508. doi:10.1128/aac.00227-10
Nett JE, Marchillo K, Spiegel CA, Andes DR (2010b) Development and validation of an in vivo Candida albicans biofilm denture model. Infect Immun 78(9):3650–3659. doi:10.1128/IAI.00480-10
Nett JE, Sanchez H, Cain MT, Andes DR (2010c) Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202(1):171–175. doi:10.1086/651200
Nett JE, Sanchez H, Cain MT, Ross KM, Andes DR (2011) Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryot Cell 10(12):1660–1669. doi:10.1128/ec.05126-11
Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, Andes DR, Mitchell AP (2008) Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18(14):1017–1024. doi:10.1016/j.cub.2008.06.034
Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, Nantel A, Andes DR, Johnson AD, Mitchell AP (2009) Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7(6), e1000133. doi:10.1371/journal.pbio.1000133
O’Toole GA (2003) To build a biofilm. J Bacteriol 185(9):2687–2689
Paulitsch AH, Willinger B, Zsalatz B, Stabentheiner E, Marth E, Buzina W (2009) In-vivo Candida biofilms in scanning electron microscopy. Med Mycol Off Publ Int Soc Human Animal Mycol 47(7):690–696. doi:10.3109/13693780802635237
Rajendran R, Williams C, Lappin DF, Millington O, Martins M, Ramage G (2013) Extracellular DNA release acts as an antifungal resistance mechanism in mature Aspergillus fumigatus biofilms. Eukaryot Cell 12(3):420–429. doi:10.1128/ec.00287-12
Ramage G, Bachmann S, Patterson TF, Wickes BL, Lopez-Ribot JL (2002) Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother 49(6):973–980
Ramage G, Rajendran R, Gutierrez-Correa M, Jones B, Williams C (2011) Aspergillus biofilms: clinical and industrial significance. FEMS Microbiol Lett 324(2):89–97. doi:10.1111/j.1574-6968.2011.02381.x
Ramage G, Rajendran R, Sherry L, Williams C (2012) Fungal biofilm resistance. Int J Microbiol 2012:528521. doi:10.1155/2012/528521
Reichhardt C, Ferreira JA, Joubert LM, Clemons KV, Stevens DA, Cegelski L (2015a) Analysis of the Aspergillus fumigatus Biofilm Extracellular Matrix by Solid-State Nuclear Magnetic Resonance Spectroscopy. Eukaryot Cell. doi:10.1128/ec.00050-15
Reichhardt C, Fong JC, Yildiz F, Cegelski L (2015b) Characterization of the Vibrio cholerae extracellular matrix: a top-down solid-state NMR approach. Biochim Biophys Acta 1848(1 Pt B):378–383. doi:10.1016/j.bbamem.2014.05.030
Reynolds TB, Fink GR (2001) Bakers’ yeast, a model for fungal biofilm formation. Science 291(5505):878–881. doi:10.1126/science.291.5505.878
Robbins N, Uppuluri P, Nett J, Rajendran R, Ramage G, Lopez-Ribot JL, Andes D, Cowen LE (2011) Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog 7(9), e1002257. doi:10.1371/journal.ppat.1002257
Roux D, Cywes-Bentley C, Zhang YF, Pons S, Konkol M, Kearns DB, Little DJ, Howell PL, Skurnik D, Pier GB (2015) Identification of Poly-N-acetylglucosamine as a Major Polysaccharide Component of the Bacillus subtilis Biofilm Matrix. J Biol Chem 290(31):19261–19272. doi:10.1074/jbc.M115.648709
Shibata N, Suzuki A, Kobayashi H, Okawa Y (2007) Chemical structure of the cell-wall mannan of Candida albicans serotype A and its difference in yeast and hyphal forms. Biochem J 404(3):365–372. doi:10.1042/BJ20070081
Shopova I, Bruns S, Thywissen A, Kniemeyer O, Brakhage AA, Hillmann F (2013) Extrinsic extracellular DNA leads to biofilm formation and colocalizes with matrix polysaccharides in the human pathogenic fungus Aspergillus fumigatus. Front Microbiol 4:141. doi:10.3389/fmicb.2013.00141
Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009) Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol Off Publ Int Soc Human Animal Mycol 47(7):681–689. doi:10.3109/13693780802549594
Srikantha T, Daniels KJ, Pujol C, Kim E, Soll DR (2013) Identification of Genes Upregulated by the Transcription Factor Bcr1 That Are Involved in Impermeability. Impenetrability and Drug-Resistance of Candida albicans a/alpha Biofilms. Eukaryot Cell. doi:10.1128/ec.00071-13
Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, Cain MT, Hamaker J, Mitchell AP, Andes DR (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
Taff HT, Mitchell KF, Edward JA, Andes DR (2013) Mechanisms of Candida biofilm drug resistance. Future Microbiol 8:1325–1337. doi:10.2217/fmb.13.101
Teschler JK, Zamorano-Sanchez D, Utada AS, Warner CJ, Wong GC, Linington RG, Yildiz FH (2015) Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol 13(5):255–268. doi:10.1038/nrmicro3433
Thomas DP, Bachmann SP, Lopez-Ribot JL (2006) Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 6(21):5795–5804. doi:10.1002/pmic.200600332
Vachova L, Stovicek V, Hlavacek O, Chernyavskiy O, Stepanek L, Kubinova L, Palkova Z (2011) Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies. J Cell Biol 194(5):679–687. doi:10.1083/jcb.201103129
Vediyappan G, Rossignol T, d’Enfert C (2010) Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob Agents Chemother 54(5):2096–2111. doi:10.1128/AAC.01638-09
Verstrepen KJ, Klis FM (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60(1):5–15. doi:10.1111/j.1365-2958.2006.05072.x
Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11(3):157–168. doi:10.1038/nrmicro2960
Yang L, Hu Y, Liu Y, Zhang J, Ulstrup J, Molin S (2011) Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13(7):1705–1717. doi:10.1111/j.1462-2920.2011.02503.x
Yi S, Sahni N, Daniels KJ, Lu KL, Srikantha T, Huang G, Garnaas AM, Soll DR (2011) Alternative mating type configurations (a/alpha versus a/a or alpha/alpha) of Candida albicans result in alternative biofilms regulated by different pathways. PLoS Biol 9(8), e1001117. doi:10.1371/journal.pbio.1001117
Zara G, Zara S, Pinna C, Marceddu S, Budroni M (2009) FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae. Microbiology 155(Pt 12):3838–3846. doi:10.1099/mic.0.028738-0
Zarnowski R, Westler WM, Lacmbouh GA, Marita JM, Bothe JR, Bernhardt J, Lounes-Hadj Sahraoui A, Fontaine J, Sanchez H, Hatfield RD, Ntambi JM, Nett JE, Mitchell AP, Andes DR (2014) Novel entries in a fungal biofilm matrix encyclopedia. mBio 5(4):e01333-14. doi:10.1128/mBio.01333-14
Zhang Y, Fonslow BR, Shan B, Baek M-C, Yates JR (2013) Protein analysis by shotgun/bottom-up proteomics. Chem Rev 113(4):2343–2394. doi:10.1021/cr3003533
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Mitchell, K.F., Zarnowski, R., Andes, D.R. (2016). The Extracellular Matrix of Fungal Biofilms. In: Imbert, C. (eds) Fungal Biofilms and related infections. Advances in Experimental Medicine and Biology(), vol 931. Springer, Cham. https://doi.org/10.1007/5584_2016_6
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