Pathogenetic Impact of Bacterial-Fungal Interactions

Filomena Nogueira, Shirin Sharghi, Karl Kuchler, Thomas Lion, Filomena Nogueira, Shirin Sharghi, Karl Kuchler, Thomas Lion

Abstract

Polymicrobial infections are of paramount importance because of the potential severity of clinical manifestations, often associated with increased resistance to antimicrobial treatment. The intricate interplay with the host and the immune system, and the impact on microbiome imbalance, are of importance in this context. The equilibrium of microbiota in the human host is critical for preventing potential dysbiosis and the ensuing development of disease. Bacteria and fungi can communicate via signaling molecules, and produce metabolites and toxins capable of modulating the immune response or altering the efficacy of treatment. Most of the bacterial-fungal interactions described to date focus on the human fungal pathogen Candida albicans and different bacteria. In this review, we discuss more than twenty different bacterial-fungal interactions involving several clinically important human pathogens. The interactions, which can be synergistic or antagonistic, both in vitro and in vivo, are addressed with a focus on the quorum-sensing molecules produced, the response of the immune system, and the impact on clinical outcome.

Keywords: bacterial–fungal interactions; immune response; in vivo models; microbiome; molecules.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1
Molecules and factors mediating the interaction between different Candida species and a variety of bacteria. Candida species include Candida (C.) albicans, Candida (C.) glabrata and Candida (C.) dubliniensis. Gram-positive bacteria are represented in lilac (Enterococcus (E.) faecalis) and Gram-negative bacteria in red (Pseudomonas (P.) aeruginosa, Escherichia (E.) coli, Acinetobacter (A.) baumannii, Aggregatibacter (A.) actinomycetemcomitans, Serratia (S.) marcescens, Bacteroides (B.) fragilis, Salmonella (S.) enterica, Klebsiella (K.) pneumoniae). Green arrows indicate supportive interactions and red lines represent inhibitory effects. If not indicated above the green arrows and red lines, the molecules mediating the interaction are currently unknown.
Figure 2
Figure 2
Molecules and factors mediating the interaction between Aspergillus species and bacteria. Aspergillus species include Aspergillus (A.) fumigatus, Aspergillus (A.) nidulans, Aspergillus (A.) niger, Aspergillus (A.) terreus and Aspergillus (A.) flavus. Gram-positive bacteria are represented in lilac (Streptomyces (S.) rapamycinicus) and Gram-negative bacteria in red (Klebsiella (K.) pneumoniae, Pseudomonas (P.) aeruginosa). Green arrows indicate supportive interactions and red lines represent inhibitory effects. If not indicated above the green arrows and red lines, the molecules mediating the interaction are currently unknown.
Figure 3
Figure 3
Molecules and factors mediating the interaction between Cryptococcus spp., Cladosporium spp., Rhizopus microsporus, Saccharomyces cerevisiae, Scedosporium aurantiacum, and different bacteria. Gram- positive bacteria are represented in lilac (Bacillus (B.) subtilis) and Gram-negative bacteria are represented in red (Pseudomonas (P.) aeruginosa, Klebsiella (K.) aerogenes). Green arrows indicate supportive interactions and red lines represent inhibitory effects. If not indicated above the green arrows and red lines, the molecules mediating the interaction are currently unknown.

References

    1. Neely A.N., Law E.J., Holder I.A. Increased susceptibility to lethal Candida infections in burned mice preinfected with Pseudomonas aeruginosa or pretreated with proteolytic enzymes. Infect. Immun. 1986;52:200–204.
    1. Bergeron A.C., Seman B.G., Hammond J.H., Archambault L.S., Hogan D.A., Wheeler R.T. Candida and Pseudomonas interact to enhance virulence of mucosal infection in transparent zebrafish. Infect. Immun. 2017 doi: 10.1128/IAI.00475-17.
    1. Kim S.H., Yoon Y.K., Kim M.J., Sohn J.W. Risk factors for and clinical implications of mixed Candida/bacterial bloodstream infections. Clin. Microbiol. Infect. 2013;19:62–68. doi: 10.1111/j.1469-0691.2012.03906.x.
    1. Wargo M.J., Hogan D.A. Fungal--bacterial interactions: a mixed bag of mingling microbes. Curr. Opin. Microbiol. 2006;9:359–364. doi: 10.1016/j.mib.2006.06.001.
    1. Peters B.M., Jabra-Rizk M.A., O’May G.A., Costerton J.W., Shirtliff M.E. Polymicrobial interactions: impact on pathogenesis and human disease. Clin. Microbiol. Rev. 2012;25:193–213. doi: 10.1128/CMR.00013-11.
    1. Diaz P.I., Strausbaugh L.D., Dongari-Bagtzoglou A. Fungal-bacterial interactions and their relevance to oral health: linking the clinic and the bench. Front. Cell. Infect. Microbiol. 2014;4:101. doi: 10.3389/fcimb.2014.00101.
    1. Hermann C., Hermann J., Munzel U., Ruchel R. Bacterial flora accompanying Candida yeasts in clinical specimens. Mycoses. 1999;42:619–627. doi: 10.1046/j.1439-0507.1999.00519.x.
    1. Morales D.K., Hogan D.A. Candida albicans interactions with bacteria in the context of human health and disease. Plos Pathog. 2010;6:1000886. doi: 10.1371/journal.ppat.1000886.
    1. Kett D.H., Azoulay E., Echeverria P.M., Vincent J.L. Candida bloodstream infections in intensive care units: analysis of the extended prevalence of infection in intensive care unit study. Crit. Care. Med. 2011;39:665–670. doi: 10.1097/CCM.0b013e318206c1ca.
    1. Thorn J.L., Gilchrist K.B., Sobonya R.E., Gaur N.K., Lipke P.N., Klotz S.A. Postmortem Candidemia: Marker of disseminated disease. J. Clin. Pathol. 2010;63:337–340. doi: 10.1136/jcp.2009.070607.
    1. De Sordi L., Muhlschlegel F.A. Quorum sensing and fungal-bacterial interactions in Candida albicans: A communicative network regulating microbial coexistence and virulence. Fems Yeast Res. 2009;9:990–999. doi: 10.1111/j.1567-1364.2009.00573.x.
    1. Dixon E.F., Hall R.A. Noisy neighbourhoods: quorum sensing in fungal-polymicrobial infections. Cell Microbiol. 2015;17:1431–1441. doi: 10.1111/cmi.12490.
    1. Braga R.M., Dourado M.N., Araujo W.L. Microbial interactions: ecology in a molecular perspective. Braz. J. Microbiol. 2016;47:86–98. doi: 10.1016/j.bjm.2016.10.005.
    1. Fischbach M.A. Microbiome: Focus on Causation and Mechanism. Cell. 2018;174:785–790. doi: 10.1016/j.cell.2018.07.038.
    1. Knight R., Vrbanac A., Taylor B.C., Aksenov A., Callewaert C., Debelius J., Gonzalez A., Kosciolek T., McCall L.I., McDonald D., et al. Best practices for analysing microbiomes. Nat. Rev. Microbiol. 2018;16:410–422. doi: 10.1038/s41579-018-0029-9.
    1. Garrett W.S. Cancer and the microbiota. Science. 2015;348:80–86. doi: 10.1126/science.aaa4972.
    1. Kruger W., Vielreicher S., Kapitan M., Jacobsen I.D., Niemiec M.J. Fungal-Bacterial Interactions in Health and Disease. Pathogens. 2019;8:70. doi: 10.3390/pathogens8020070.
    1. Marsland B.J., Gollwitzer E.S. Host-microorganism interactions in lung diseases. Nat. Rev. Immunol. 2014;14:827–835. doi: 10.1038/nri3769.
    1. Nash A.K., Auchtung T.A., Wong M.C., Smith D.P., Gesell J.R., Ross M.C., Stewart C.J., Metcalf G.A., Muzny D.M., Gibbs R.A., et al. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome. 2017;5:153. doi: 10.1186/s40168-017-0373-4.
    1. Witherden E.A., Shoaie S., Hall R.A., Moyes D.L. The Human Mucosal Mycobiome and Fungal Community Interactions. J. Fungi (Basel) 2017;3:56. doi: 10.3390/jof3040056.
    1. Jo J.H., Kennedy E.A., Kong H.H. Topographical and physiological differences of the skin mycobiome in health and disease. Virulence. 2017;8:324–333. doi: 10.1080/21505594.2016.1249093.
    1. Statovci D., Aguilera M., MacSharry J., Melgar S. The Impact of Western Diet and Nutrients on the Microbiota and Immune Response at Mucosal Interfaces. Front. Immunol. 2017;8:838. doi: 10.3389/fimmu.2017.00838.
    1. Clarke G., Stilling R.M., Kennedy P.J., Stanton C., Cryan J.F., Dinan T.G. Minireview: Gut microbiota: the neglected endocrine organ. Mol. Endocrinol. 2014;28:1221–1238. doi: 10.1210/me.2014-1108.
    1. Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Cell. 2014;157:121–141. doi: 10.1016/j.cell.2014.03.011.
    1. Caballero S., Pamer E.G. Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu. Rev. Immunol. 2015;33:227–256. doi: 10.1146/annurev-immunol-032713-120238.
    1. Selber-Hnatiw S., Rukundo B., Ahmadi M., Akoubi H., Al-Bizri H., Aliu A.F., Ambeaghen T.U., Avetisyan L., Bahar I., Baird A. Human Gut Microbiota: Toward an Ecology of Disease. Front. Microbiol. 2017;8:1265. doi: 10.3389/fmicb.2017.01265.
    1. Tojo R., Suarez A., Clemente M.G., de los Reyes-Gavilan C.G., Margolles A., Gueimonde M., Ruas-Madiedo P. Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 2014;20:15163–15176. doi: 10.3748/wjg.v20.i41.15163.
    1. Candela M., Turroni S., Biagi E., Carbonero F., Rampelli S., Fiorentini C., Brigidi P. Inflammation and colorectal cancer, when microbiota-host mutualism breaks. World J. Gastroenterol. 2014;20:908–922. doi: 10.3748/wjg.v20.i4.908.
    1. Galloway-Pena J., Brumlow C., Shelburne S. Impact of the Microbiota on Bacterial Infections during Cancer Treatment. Trends Microbiol. 2017;25:992–1004. doi: 10.1016/j.tim.2017.06.006.
    1. Heisel T., Montassier E., Johnson A., Al-Ghalith G., Lin Y.W., Wei L.N., Knights D., Gale C.A. High-Fat Diet Changes Fungal Microbiomes and Interkingdom Relationships in the Murine Gut. mSphere. 2017;2 doi: 10.1128/mSphere.00351-17.
    1. Lof M., Janus M.M., Krom B.P. Metabolic Interactions between Bacteria and Fungi in Commensal Oral Biofilms. J. Fungi (Basel) 2017;3:40. doi: 10.3390/jof3030040.
    1. Raskov H., Burcharth J., Pommergaard H.C. Linking Gut Microbiota to Colorectal Cancer. J. Cancer. 2017;8:3378–3395. doi: 10.7150/jca.20497.
    1. Tsilimigras M.C., Fodor A., Jobin C. Carcinogenesis and therapeutics: the microbiota perspective. Nat. Microbiol. 2017;2:17008. doi: 10.1038/nmicrobiol.2017.8.
    1. Zitvogel L., Daillere R., Roberti M.P., Routy B., Kroemer G. Anticancer effects of the microbiome and its products. Nat. Rev. Microbiol. 2017;15:465–478. doi: 10.1038/nrmicro.2017.44.
    1. Schwabe R.F., Jobin C. The microbiome and cancer. Nat. Rev. Cancer. 2013;13:800–812. doi: 10.1038/nrc3610.
    1. Liguori G., Lamas B., Richard M.L., Brandi G., da Costa G., Hoffmann T.W., Di Simone M.P., Calabrese C., Poggioli G., Langella P., et al. Fungal Dysbiosis in Mucosa-associated Microbiota of Crohn’s Disease Patients. J. Crohns. Colitis. 2016;10:296–305. doi: 10.1093/ecco-jcc/jjv209.
    1. Pope J.L., Tomkovich S., Yang Y., Jobin C. Microbiota as a mediator of cancer progression and therapy. Transl. Res. 2017;179:139–154. doi: 10.1016/j.trsl.2016.07.021.
    1. Gagniere J., Raisch J., Veziant J., Barnich N., Bonnet R., Buc E., Bringer M.A., Pezet D., Bonnet M. Gut microbiota imbalance and colorectal cancer. World J. Gastroenterol. 2016;22:501–518. doi: 10.3748/wjg.v22.i2.501.
    1. DeGruttola A.K., Low D., Mizoguchi A., Mizoguchi E. Current Understanding of Dysbiosis in Disease in Human and Animal Models. Inflamm. Bowel Dis. 2016;22:1137–1150. doi: 10.1097/MIB.0000000000000750.
    1. Williams S.C. Gnotobiotics. Proc. Natl. Acad. Sci. USA. 2014;111:1661. doi: 10.1073/pnas.1324049111.
    1. Gordon H.A., Pesti L. The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriol. Rev. 1971;35:390–429.
    1. Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon J.I. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009;1:6ra14. doi: 10.1126/scitranslmed.3000322.
    1. Gill S.R., Pop M., Deboy R.T., Eckburg P.B., Turnbaugh P.J., Samuel B.S., Gordon J.I., Relman D.A., Fraser-Liggett C.M., Nelson K.E. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–1359. doi: 10.1126/science.1124234.
    1. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–1031. doi: 10.1038/nature05414.
    1. Backhed F., Ding H., Wang T., Hooper L.V., Koh G.Y., Nagy A., Semenkovich C.F., Gordon J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA. 2004;101:15718–15723. doi: 10.1073/pnas.0407076101.
    1. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science. 2006;313:1126–1130. doi: 10.1126/science.1127119.
    1. Umesaki Y. Use of gnotobiotic mice to identify and characterize key microbes responsible for the development of the intestinal immune system. Proc. Jpn. Acad. Ser. B. 2014;90:313–332. doi: 10.2183/pjab.90.313.
    1. Burmolle M., Ren D., Bjarnsholt T., Sorensen S.J. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 2014;22:84–91. doi: 10.1016/j.tim.2013.12.004.
    1. de Vos W.M. Microbial biofilms and the human intestinal microbiome. Npj Biofilms Microbiomes. 2015;1:15005. doi: 10.1038/npjbiofilms.2015.5.
    1. Raskov H., Kragh K.N., Bjarnsholt T., Alamili M., Gogenur I. Bacterial biofilm formation inside colonic crypts may accelerate colorectal carcinogenesis. Clin. Transl. Med. 2018;7:018–0209. doi: 10.1186/s40169-018-0209-2.
    1. Leclair L.W., Hogan D.A. Mixed bacterial-fungal infections in the, C.F. respiratory tract. Med. Mycol. 2010;48:521522. doi: 10.3109/13693786.2010.521522.
    1. Chotirmall S.H., O’Donoghue E., Bennett K., Gunaratnam C., O’Neill S.J., McElvaney N.G. Sputum Candida albicans presages, F.E.V(1) decline and hospital-treated exacerbations in cystic fibrosis. Chest. 2010;138:1186–1195. doi: 10.1378/chest.09-2996.
    1. Reece E., Segurado R., Jackson A., McClean S., Renwick J., Greally P. Co-colonisation with Aspergillus fumigatus and Pseudomonas aeruginosa is associated with poorer health in cystic fibrosis patients: an Irish registry analysis. BMC Pulm. Med. 2017;17:70. doi: 10.1186/s12890-017-0416-4.
    1. Fujimura K.E., Sitarik A.R., Havstad S., Lin D.L., Levan S., Fadrosh D., Panzer A.R., LaMere B., Rackaityte E., Lukacs N.W., et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat. Med. 2016;22:1187–1191. doi: 10.1038/nm.4176.
    1. Arrieta M.C., Stiemsma L.T., Dimitriu P.A., Thorson L., Russell S., Yurist-Doutsch S., Kuzeljevic B., Gold M.J., Britton H.M., Lefebvre D.L., et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 2015;7:307ra152. doi: 10.1126/scitranslmed.aab2271.
    1. Sobel J.D. Vulvovaginal candidosis. Lancet. 2007;369:1961–1971. doi: 10.1016/S0140-6736(07)60917-9.
    1. van de Wijgert J.H., Borgdorff H., Verhelst R., Crucitti T., Francis S., Verstraelen H., Jespers V. The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS ONE. 2014;9:e105998. doi: 10.1371/journal.pone.0105998.
    1. Hall R.A., Noverr M.C. Fungal interactions with the human host: exploring the spectrum of symbiosis. Curr. Opin. Microbiol. 2017;40:58–64. doi: 10.1016/j.mib.2017.10.020.
    1. Burd R.S., Raymond C.S., Dunn D.L. Endotoxin promotes synergistic lethality during concurrent Escherichia coli and Candida albicans infection. J. Surg. Res. 1992;52:537–542. doi: 10.1016/0022-4804(92)90125-J.
    1. Ikeda T., Suegara N., Abe S., Yamaguchi H. Efficacy of antibacterial drugs in mice with complex infection by Candida albicans and Escherichia coli. J. Antibiot. 1999;52:552–558. doi: 10.7164/antibiotics.52.552.
    1. Standaert-Vitse A., Sendid B., Joossens M., Francois N., Vandewalle-El Khoury P., Branche J., Van Kruiningen H., Jouault T., Rutgeerts P., Gower-Rousseau C., et al. Candida albicans colonization and, in familial Crohn’s disease. Am. J. Gastroenterol. 2009;104:1745–1753. doi: 10.1038/ajg.2009.225.
    1. Chiaro T.R., Soto R., Zac Stephens W., Kubinak J.L., Petersen C., Gogokhia L., Bell R., Delgado J.C., Cox J., Voth W., et al. A member of the gut mycobiota modulates host purine metabolism exacerbating colitis in mice. Sci. Transl. Med. 2017;9 doi: 10.1126/scitranslmed.aaf9044.
    1. Qiu X., Zhang F., Yang X., Wu N., Jiang W., Li X., Liu Y. Changes in the composition of intestinal fungi and their role in mice with dextran sulfate sodium-induced colitis. Sci. Rep. 2015;5:10416. doi: 10.1038/srep10416.
    1. Noverr M.C., Noggle R.M., Toews G.B., Huffnagle G.B. Role of antibiotics and fungal microbiota in driving pulmonary allergic responses. Infect. Immun. 2004;72:4996–5003. doi: 10.1128/IAI.72.9.4996-5003.2004.
    1. Wheeler M.L., Limon J.J., Bar A.S., Leal C.A., Gargus M., Tang J., Brown J., Funari V.A., Wang H.L., Crother T.R., et al. Immunological Consequences of Intestinal Fungal Dysbiosis. Cell Host Microbe. 2016;19:865–873. doi: 10.1016/j.chom.2016.05.003.
    1. Sommer F., Backhed F. The gut microbiota--masters of host development and physiology. Nat. Rev. Microbiol. 2013;11:227–238. doi: 10.1038/nrmicro2974.
    1. Singh N., Gurav A., Sivaprakasam S., Brady E., Padia R., Shi H., Thangaraju M., Prasad P.D., Manicassamy S., Munn D.H., et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40:128–139. doi: 10.1016/j.immuni.2013.12.007.
    1. Louis P., Flint H.J. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 2009;294:1–8. doi: 10.1111/j.1574-6968.2009.01514.x.
    1. Li J., Butcher J., Mack D., Stintzi A. Functional impacts of the intestinal microbiome in the pathogenesis of inflammatory bowel disease. Inflamm. Bowel Dis. 2015;21:139–153. doi: 10.1097/MIB.0000000000000215.
    1. Sam Q.H., Chang M.W., Chai L.Y. The Fungal Mycobiome and Its Interaction with Gut Bacteria in the Host. Int. J. Mol. Sci. 2017;18:330. doi: 10.3390/ijms18020330.
    1. Nguyen G.C. Editorial: bugs and drugs: insights into the pathogenesis of inflammatory bowel disease. Am. J. Gastroenterol. 2011;106:2143–2145. doi: 10.1038/ajg.2011.308.
    1. Schulz M.D., Atay C., Heringer J., Romrig F.K., Schwitalla S., Aydin B., Ziegler P.K., Varga J., Reindl W., Pommerenke C., et al. High-fat-diet-mediated dysbiosis promotes intestinal carcinogenesis independently of obesity. Nature. 2014;514:508–512. doi: 10.1038/nature13398.
    1. Belcheva A., Irrazabal T., Robertson S.J., Streutker C., Maughan H., Rubino S., Moriyama E.H., Copeland J.K., Surendra A., Kumar S., et al. Gut microbial metabolism drives transformation of, M.S.H2-deficient colon epithelial cells. Cell. 2014;158:288–299. doi: 10.1016/j.cell.2014.04.051.
    1. Lupton J.R. Microbial degradation products influence colon cancer risk: the butyrate controversy. J. Nutr. 2004;134:479–482. doi: 10.1093/jn/134.2.479.
    1. Palmer K.L., Aye L.M., Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J. Bacteriol. 2007;189:8079–8087. doi: 10.1128/JB.01138-07.
    1. Gainza-Cirauqui M.L., Nieminen M.T., Novak Frazer L., Aguirre-Urizar J.M., Moragues M.D., Rautemaa R. Production of carcinogenic acetaldehyde by Candida albicans from patients with potentially malignant oral mucosal disorders. J. Oral Pathol. Med. 2013;42:243–249. doi: 10.1111/j.1600-0714.2012.01203.x.
    1. Meurman J.H., Uittamo J. Oral micro-organisms in the etiology of cancer. Acta. Odontol. Scand. 2008;66:321–326. doi: 10.1080/00016350802446527.
    1. Whiteley M., Diggle S.P., Greenberg E.P. Progress in and promise of bacterial quorum sensing research. Nature. 2017;551:313–320. doi: 10.1038/nature24624.
    1. Rio R.V.M. Don’t Bite the Hand that Feeds You. Cell Host Microbe. 2017;21:552–554. doi: 10.1016/j.chom.2017.04.013.
    1. Polke M., Jacobsen I.D. Quorum sensing by farnesol revisited. Curr. Genet. 2017;63:791–797. doi: 10.1007/s00294-017-0683-x.
    1. Papenfort K., Bassler B.L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 2016;14:576–588. doi: 10.1038/nrmicro.2016.89.
    1. O’Toole G.A. Classic Spotlight: Quorum Sensing and the Multicellular Life of Unicellular Organisms. J. Bacteriol. 2016;198:601. doi: 10.1128/JB.00956-15.
    1. Hofer U. Biofilms: Turning tides for quorum sensing. Nat. Rev. Microbiol. 2016;14:64. doi: 10.1038/nrmicro.2015.26.
    1. Pammi M., Liang R., Hicks J., Mistretta T.A., Versalovic J. Biofilm extracellular, D.N.A enhances mixed species biofilms of Staphylococcus epidermidis and Candida albicans. BMC Microbiol. 2013;13:1471–2180. doi: 10.1186/1471-2180-13-257.
    1. Smith K., Rajendran R., Kerr S., Lappin D.F., Mackay W.G., Williams C., Ramage G. Aspergillus fumigatus enhances elastase production in Pseudomonas aeruginosa co-cultures. Med. Mycol. 2015;53:645–655. doi: 10.1093/mmy/myv048.
    1. Mear J.B., Kipnis E., Faure E., Dessein R., Schurtz G., Faure K., Guery B. Candida albicans and Pseudomonas aeruginosa interactions: more than an opportunistic criminal association? Med. Mal. Infect. 2013;43:146–151. doi: 10.1016/j.medmal.2013.02.005.
    1. Tan C.H., Koh K.S., Xie C., Zhang J., Tan X.H., Lee G.P., Zhou Y., Ng W.J., Rice S.A., Kjelleberg S. Community quorum sensing signalling and quenching: microbial granular biofilm assembly. Npj Biofilms Microbiomes. 2015;1:15006. doi: 10.1038/npjbiofilms.2015.6.
    1. Dong Y.H., Xu J.L., Li X.Z., Zhang L.H. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA. 2000;97:3526–3531. doi: 10.1073/pnas.97.7.3526.
    1. Defoirdt T. Quorum-Sensing Systems as Targets for Antivirulence Therapy. Trends Microbiol. 2017 doi: 10.1016/j.tim.2017.10.005.
    1. Abraham W.R. Going beyond the Control of Quorum-Sensing to Combat Biofilm Infections. Antibiotics (Basel) 2016;5:3. doi: 10.3390/antibiotics5010003.
    1. Thompson J.A., Oliveira R.A., Djukovic A., Ubeda C., Xavier K.B. Manipulation of the quorum sensing signal, A.I.-2 affects the antibiotic-treated gut microbiota. Cell Rep. 2015;10:1861–1871. doi: 10.1016/j.celrep.2015.02.049.
    1. Garcia-Contreras R. Is Quorum Sensing Interference a Viable Alternative to Treat Pseudomonas aeruginosa Infections? Front. Microbiol. 2016;7:1454. doi: 10.3389/fmicb.2016.01454.
    1. Guo Q., Wei Y., Xia B., Jin Y., Liu C., Pan X., Shi J., Zhu F., Li J., Qian L., et al. Identification of a small molecule that simultaneously suppresses virulence and antibiotic resistance of Pseudomonas aeruginosa. Sci. Rep. 2016;6:19141. doi: 10.1038/srep19141.
    1. Muimhneacháin E.Ó., Reen F.J., O’Gara F., McGlacken G.P. Analogues of Pseudomonas aeruginosa signalling molecules to tackle infections. Org. Biomol. Chem. 2018;16:169–179. doi: 10.1039/C7OB02395B.
    1. Smith A.C., Rice A., Sutton B., Gabrilska R., Wessel A.K., Whiteley M., Rumbaugh K.P. Albumin Inhibits Pseudomonas aeruginosa Quorum Sensing and Alters Polymicrobial Interactions. Infect. Immun. 2017;85:116. doi: 10.1128/IAI.00116-17.
    1. Imperi F., Leoni L., Visca P. Antivirulence activity of azithromycin in Pseudomonas aeruginosa. Front. Microbiol. 2014;5:178. doi: 10.3389/fmicb.2014.00178.
    1. Ramage G., Saville S.P., Wickes B.L., Lopez-Ribot J.L. Inhibition of Candida albicans Biofilm Formation by Farnesol, a Quorum-Sensing Molecule. Appl. Environ. Microbiol. 2002;68:5459–5463. doi: 10.1128/AEM.68.11.5459-5463.2002.
    1. Cordeiro R.A., Teixeira C.E., Brilhante R.S., Castelo-Branco D.S., Paiva M.A., Giffoni Leite J.J., Lima D.T., Monteiro A.J., Sidrim J.J., Rocha M.F. Minimum inhibitory concentrations of amphotericin B, azoles and caspofungin against Candida species are reduced by farnesol. Med. Mycol. 2013;51:53–59. doi: 10.3109/13693786.2012.692489.
    1. Mear J.B., Gosset P., Kipnis E., Faure E., Dessein R., Jawhara S., Fradin C., Faure K., Poulain D., Sendid B., et al. Candida albicans airway exposure primes the lung innate immune response against Pseudomonas aeruginosa infection through innate lymphoid cell recruitment and interleukin-22-associated mucosal response. Infect. Immun. 2014;82:306–315. doi: 10.1128/IAI.01085-13.
    1. Peleg A.Y., Hogan D.A., Mylonakis E. Medically important bacterial-fungal interactions. Nat. Rev. Microbiol. 2010;8:340–349. doi: 10.1038/nrmicro2313.
    1. Gibson J., Sood A., Hogan D.A. Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl. Env. Microbiol. 2009;75:504–513. doi: 10.1128/AEM.01037-08.
    1. Hogan D.A., Vik A., Kolter R. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 2004;54:1212–1223. doi: 10.1111/j.1365-2958.2004.04349.x.
    1. Hogan D.A. Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot. Cell. 2006;5:613–619. doi: 10.1128/EC.5.4.613-619.2006.
    1. Purschke F.G., Hiller E., Trick I., Rupp S. Flexible survival strategies of Pseudomonas aeruginosa in biofilms result in increased fitness compared with Candida albicans. Mol. Cell Proteomics. 2012;11:1652–1669. doi: 10.1074/mcp.M112.017673.
    1. Kerr J.R. Suppression of fungal growth exhibited by Pseudomonas aeruginosa. J. Clin. Microbiol. 1994;32:525–527.
    1. Kerr J.R., Taylor G.W., Rutman A., Hoiby N., Cole P.J., Wilson R. Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J. Clin. Pathol. 1999;52:385–387. doi: 10.1136/jcp.52.5.385.
    1. Charlton T.S., de Nys R., Netting A., Kumar N., Hentzer M., Givskov M., Kjelleberg S. A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Env. Microbiol. 2000;2:530–541. doi: 10.1046/j.1462-2920.2000.00136.x.
    1. Hogan D.A., Kolter R. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science. 2002;296:2229–2232. doi: 10.1126/science.1070784.
    1. Cugini C., Calfee M.W., Farrow J.M., 3rd, Morales D.K., Pesci E.C., Hogan D.A. Farnesol, a common sesquiterpene, inhibits, P.Q.S production in Pseudomonas aeruginosa. Mol. Microbiol. 2007;65:896–906. doi: 10.1111/j.1365-2958.2007.05840.x.
    1. Chen A.I., Dolben E.F., Okegbe C., Harty C.E., Golub Y., Thao S., Ha D.G., Willger S.D., O’Toole G.A., Harwood C.S., et al. Candida albicans ethanol stimulates Pseudomonas aeruginosa WspR-controlled biofilm formation as part of a cyclic relationship involving phenazines. PloS Pathog. 2014;10:e1004480. doi: 10.1371/journal.ppat.1004480.
    1. Fourie R., Pohl C.H. Beyond Antagonism: The Interaction Between Candida Species and Pseudomonas aeruginosa. J. Fungi (Basel) 2019;5:34. doi: 10.3390/jof5020034.
    1. Cavalcanti I.M., Del Bel Cury A.A., Jenkinson H.F., Nobbs A.H. Interactions between Streptococcus oralis, Actinomyces oris, and Candida albicans in the development of multispecies oral microbial biofilms on salivary pellicle. Mol. Oral Microbiol. 2017;32:60–73. doi: 10.1111/omi.12154.
    1. Xu H., Sobue T., Thompson A., Xie Z., Poon K., Ricker A., Cervantes J., Diaz P.I., Dongari-Bagtzoglou A. Streptococcal co-infection augments Candida pathogenicity by amplifying the mucosal inflammatory response. Cell Microbiol. 2014;16:214–231. doi: 10.1111/cmi.12216.
    1. Holmes A.R., Gopal P.K., Jenkinson H.F. Adherence of Candida albicans to a cell surface polysaccharide receptor on Streptococcus gordonii. Infect. Immun. 1995;63:1827–1834.
    1. Holmes A.R., McNab R., Jenkinson H.F. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect. Immun. 1996;64:4680–4685.
    1. Nobbs A.H., Vickerman M.M., Jenkinson H.F. Heterologous expression of Candida albicans cell wall-associated adhesins in Saccharomyces cerevisiae Reveals differential specificities in adherence and biofilm formation and in binding oral Streptococcus gordonii. Eukaryot. Cell. 2010;9:1622–1634. doi: 10.1128/EC.00103-10.
    1. Jenkinson H.F., Lala H.C., Shepherd M.G. Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect. Immun. 1990;58:1429–1436.
    1. O’Sullivan J.M., Jenkinson H.F., Cannon R.D. Adhesion of Candida albicans to oral streptococci is promoted by selective adsorption of salivary proteins to the streptococcal cell surface. Microbiology. 2000;146:41–48. doi: 10.1099/00221287-146-1-41.
    1. Kim D., Sengupta A., Niepa T.H., Lee B.H., Weljie A., Freitas-Blanco V.S., Murata R.M., Stebe K.J., Lee D., Koo H. Candida albicans stimulates Streptococcus mutans microcolony development via cross-kingdom biofilm-derived metabolites. Sci. Rep. 2017;7:41332. doi: 10.1038/srep41332.
    1. Montelongo-Jauregui D., Saville S.P., Lopez-Ribot J.L. Contributions of Candida albicans Dimorphism, Adhesive Interactions, and Extracellular Matrix to the Formation of Dual-Species Biofilms with Streptococcus gordonii. Mbio. 2019;10:e01179-19. doi: 10.1128/mBio.01179-19.
    1. Holmes A.R., van der Wielen P., Cannon R.D., Ruske D., Dawes P. Candida albicans binds to saliva proteins selectively adsorbed to silicone. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2006;102:488–494. doi: 10.1016/j.tripleo.2005.10.052.
    1. Bamford C.V., d’Mello A., Nobbs A.H., Dutton L.C., Vickerman M.M., Jenkinson H.F. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect. Immun. 2009;77:3696–3704. doi: 10.1128/IAI.00438-09.
    1. Yu X.Y., Fu F., Kong W.N., Xuan Q.K., Wen D.H., Chen X.Q., He Y.M., He L.H., Guo J., Zhou A.P., et al. Streptococcus agalactiae Inhibits Candida albicans Hyphal Development and Diminishes Host Vaginal Mucosal, T.H.17 Response. Front. Microbiol. 2018;9:198. doi: 10.3389/fmicb.2018.00198.
    1. Vilchez R., Lemme A., Ballhausen B., Thiel V., Schulz S., Jansen R., Sztajer H., Wagner-Döbler I. Streptococcus mutans inhibits Candida albicans hyphal formation by the fatty acid signaling molecule trans-2-decenoic acid (SDSF) Chembiochem. 2010;11:1552–1562. doi: 10.1002/cbic.201000086.
    1. Jarosz L.M., Deng D.M., van der Mei H.C., Crielaard W., Krom B.P. Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot. Cell. 2009;8:1658–1664. doi: 10.1128/EC.00070-09.
    1. Ahn S.J., Wen Z.T., Burne R.A. Multilevel control of competence development and stress tolerance in Streptococcus mutans, U.A.159. Infect. Immun. 2006;74:1631–1642. doi: 10.1128/IAI.74.3.1631-1642.2006.
    1. Kong E.F., Tsui C., Kucharikova S., Andes D., Van Dijck P., Jabra-Rizk M.A. Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix. Mbio. 2016;7 doi: 10.1128/mBio.01365-16.
    1. Pate J.C., Jones D.B., Wilhelmus K.R. Prevalence and spectrum of bacterial co-infection during fungal keratitis. Br. J. Ophthalmol. 2006;90:289–292. doi: 10.1136/bjo.2005.081869.
    1. Gupta N., Haque A., Mukhopadhyay G., Narayan R.P., Prasad R. Interactions between bacteria and Candida in the burn wound. Burns. 2005;31:375–378. doi: 10.1016/j.burns.2004.11.012.
    1. Klotz S.A., Chasin B.S., Powell B., Gaur N.K., Lipke P.N. Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Diagn. Microbiol. Infect. Dis. 2007;59:401–406. doi: 10.1016/j.diagmicrobio.2007.07.001.
    1. Schlecht L.M., Peters B.M., Krom B.P., Freiberg J.A., Hansch G.M., Filler S.G., Jabra-Rizk M.A., Shirtliff M.E. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology. 2015;161:168–181. doi: 10.1099/mic.0.083485-0.
    1. Krause J., Geginat G., Tammer I. Prostaglandin E2 from Candida albicans Stimulates the Growth of Staphylococcus aureus in Mixed Biofilms. PLoS ONE. 2015;10:e0135404. doi: 10.1371/journal.pone.0135404.
    1. Shirtliff M.E., Peters B.M., Jabra-Rizk M.A. Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol. Lett. 2009;299:1–8. doi: 10.1111/j.1574-6968.2009.01668.x.
    1. Kong E.F., Tsui C., Kucharikova S., Van Dijck P., Jabra-Rizk M.A. Modulation of Staphylococcus aureus Response to Antimicrobials by the Candida albicans Quorum Sensing Molecule Farnesol. Antimicrob. Agents Chemother. 2017;61:e01573-17. doi: 10.1128/AAC.01573-17.
    1. Inoue Y., Shiraishi A., Hada T., Hirose K., Hamashima H., Shimada J. The antibacterial effects of terpene alcohols on Staphylococcus aureus and their mode of action. FEMS Microbiol. Lett. 2004;237:325–331. doi: 10.1111/j.1574-6968.2004.tb09714.x.
    1. Jabra-Rizk M.A., Meiller T.F., James C.E., Shirtliff M.E. Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial susceptibility. Antimicrob. Agents Chemother. 2006;50:1463–1469. doi: 10.1128/AAC.50.4.1463-1469.2006.
    1. Camarillo-Marquez O., Cordova-Alcantara I.M., Hernandez-Rodriguez C.H., Garcia-Perez B.E., Martinez-Rivera M.A., Rodríguez-Tovar A.V. Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism. Front. Microbiol. 2018;9:2031. doi: 10.3389/fmicb.2018.02031.
    1. Garsin D.A., Lorenz M.C. Candida albicans and Enterococcus faecalis in the gut: synergy in commensalism? Gut Microbes. 2013;4:409–415. doi: 10.4161/gmic.26040.
    1. Kovac J., Kovac D., Slobodnikova L., Kotulova D. Enterococcus faecalis and Candida albicans in the dental root canal and periapical infections. Bratisl. Lek. Listy. 2013;114:716–720.
    1. Cruz M.R., Graham C.E., Gagliano B.C., Lorenz M.C., Garsin D.A. Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect. Immun. 2013;81:189–200. doi: 10.1128/IAI.00914-12.
    1. Graham C.E., Cruz M.R., Garsin D.A., Lorenz M.C. Enterococcus faecalis bacteriocin EntV inhibits hyphal morphogenesis, biofilm formation, and virulence of Candida albicans. Proc. Natl. Acad. Sci. USA. 2017;114:4507–4512. doi: 10.1073/pnas.1620432114.
    1. Shekh R.M., Roy U. Biochemical characterization of an anti-Candida factor produced by Enterococcus faecalis. BMC Microbiol. 2012;12:1471–2180. doi: 10.1186/1471-2180-12-132.
    1. Dutton L.C., Jenkinson H.F., Lamont R.J., Nobbs A.H. Role of Candida albicans secreted aspartyl protease Sap9 in interkingdom biofilm formation. Pathog. Dis. 2016;74:14. doi: 10.1093/femspd/ftw005.
    1. Boris S., Barbes C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2000;2:543–546. doi: 10.1016/S1286-4579(00)00313-0.
    1. Noverr M.C., Huffnagle G.B. Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect. Immun. 2004;72:6206–6210. doi: 10.1128/IAI.72.11.6206-6210.2004.
    1. Vylkova S., Carman A.J., Danhof H.A., Collette J.R., Zhou H., Lorenz M.C. The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. Mbio. 2011;2:e00055-11. doi: 10.1128/mBio.00055-11.
    1. Wang S., Wang Q., Yang E., Yan L., Li T., Zhuang H. Antimicrobial Compounds Produced by Vaginal Lactobacillus crispatus Are Able to Strongly Inhibit Candida albicans Growth, Hyphal Formation and Regulate Virulence-related Gene Expressions. Front. Microbiol. 2017;8:564. doi: 10.3389/fmicb.2017.00564.
    1. Grimaudo N.J., Nesbitt W.E., Clark W.B. Coaggregation of Candida albicans with oral Actinomyces species. Oral Microbiol. Immunol. 1996;11:59–61. doi: 10.1111/j.1399-302X.1996.tb00337.x.
    1. Arzmi M.H., Dashper S., Catmull D., Cirillo N., Reynolds E.C., McCullough M. Coaggregation of Candida albicans, Actinomyces naeslundii and Streptococcus mutans is Candida albicans strain dependent. FEMS Yeast Res. 2015;15:7. doi: 10.1093/femsyr/fov038.
    1. Arzmi M.H., Alnuaimi A.D., Dashper S., Cirillo N., Reynolds E.C., McCullough M. Polymicrobial biofilm formation by Candida albicans, Actinomyces naeslundii, and Streptococcus mutans is Candida albicans strain and medium dependent. Med. Mycol. 2016;54:856–864. doi: 10.1093/mmy/myw042.
    1. Deng L., Li W., He Y., Wu J., Ren B., Zou L. Cross-kingdom interaction of Candida albicans and Actinomyces viscosus elevated cariogenic virulence. Arch. Oral Biol. 2019;100:106–112. doi: 10.1016/j.archoralbio.2019.02.008.
    1. Peleg A.Y., Seifert H., Paterson D.L. Acinetobacter baumannii: emergence of a successful pathogen. Clin. Microbiol. Rev. 2008;21:538–582. doi: 10.1128/CMR.00058-07.
    1. Peleg A.Y., Tampakakis E., Fuchs B.B., Eliopoulos G.M., Moellering R.C., Jr., Mylonakis E. Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 2008;105:14585–14590. doi: 10.1073/pnas.0805048105.
    1. Gaddy J.A., Tomaras A.P., Actis L.A. The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect. Immun. 2009;77:3150–3160. doi: 10.1128/IAI.00096-09.
    1. Kostoulias X., Murray G.L., Cerqueira G.M., Kong J.B., Bantun F., Mylonakis E., Khoo C.A., Peleg A.Y. Impact of a Cross-Kingdom Signaling Molecule of Candida albicans on Acinetobacter baumannii Physiology. Antimicrob. Agents Chemother. 2015;60:161–167. doi: 10.1128/AAC.01540-15.
    1. Liu C.Y., Liao C.H., Chen Y.C., Chang S.C. Changing epidemiology of nosocomial bloodstream infections in 11 teaching hospitals in Taiwan between 1993 and 2006. J. Microbiol. Immunol. Infect. 2010;43:416–429. doi: 10.1016/S1684-1182(10)60065-5.
    1. Bachtiar E.W., Bachtiar B.M., Jarosz L.M., Amir L.R., Sunarto H., Ganin H., Meijler M.M., Krom B.P. AI-2 of Aggregatibacter actinomycetemcomitans inhibits Candida albicans biofilm formation. Front. Cell Infect. Microbiol. 2014;4:94. doi: 10.3389/fcimb.2014.00094.
    1. Brusca M.I., Rosa A., Albaina O., Moragues M.D., Verdugo F., Pontón J. The impact of oral contraceptives on women’s periodontal health and the subgingival occurrence of aggressive periodontopathogens and Candida species. J. Periodontol. 2010;81:1010–1018. doi: 10.1902/jop.2010.090575.
    1. Rickard A.H., Campagna S.R., Kolenbrander P.E. Autoinducer-2 is produced in saliva-fed flow conditions relevant to natural oral biofilms. J. Appl. Microbiol. 2008;105:2096–2103. doi: 10.1111/j.1365-2672.2008.03910.x.
    1. Carlson E. Enhancement by Candida albicans of Staphylococcus aureus, Serratia marcescens, and Streptococcus faecalis in the establishment of infection in mice. Infect. Immun. 1983;39:193–197.
    1. Bagg J., Silverwood R.W. Coagglutination reactions between Candida albicans and oral bacteria. J. Med. Microbiol. 1986;22:165–169. doi: 10.1099/00222615-22-2-165.
    1. Grimaudo N.J., Nesbitt W.E. Coaggregation of Candida albicans with oral Fusobacterium species. Oral Microbiol. Immunol. 1997;12:168–173. doi: 10.1111/j.1399-302X.1997.tb00374.x.
    1. Jabra-Rizk M.A., Falkler W.A., Jr., Merz W.G., Kelley J.I., Baqui A.A., Meiller T.F. Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J. Clin. Microbiol. 1999;37:1464–1468.
    1. Bor B., Cen L., Agnello M., Shi W., He X. Morphological and physiological changes induced by contact-dependent interaction between Candida albicans and Fusobacterium nucleatum. Sci. Rep. 2016;6:27956. doi: 10.1038/srep27956.
    1. Wu T., Cen L., Kaplan C., Zhou X., Lux R., Shi W., He X. Cellular Components Mediating Coadherence of Candida albicans and Fusobacterium nucleatum. J. Dent. Res. 2015;94:1432–1438. doi: 10.1177/0022034515593706.
    1. Baldwin A., Mahenthiralingam E., Drevinek P., Vandamme P., Govan J.R., Waine D.J., LiPuma J.J., Chiarini L., Dalmastri C., Henry D.A., et al. Environmental Burkholderia cepacia complex isolates in human infections. Emerg. Infect. Dis. 2007;13:458–461. doi: 10.3201/eid1303.060403.
    1. Sousa S.A., Ramos C.G., Leitao J.H. Burkholderia cepacia Complex: Emerging Multihost Pathogens Equipped with a Wide Range of Virulence Factors and Determinants. Int. J. Microbiol. 2011;10:3. doi: 10.1155/2011/607575.
    1. Boon C., Deng Y., Wang L.H., He Y., Xu J.L., Fan Y., Pan S.Q., Zhang L.H. A novel, D.S.F-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2008;2:27–36. doi: 10.1038/ismej.2007.76.
    1. Tian J., Weng L.X., Zhang Y.Q., Wang L.H. BDSF inhibits Candida albicans adherence to urinary catheters. Microb. Pathog. 2013;64:33–38. doi: 10.1016/j.micpath.2013.07.003.
    1. Fox E.P., Cowley E.S., Nobile C.J., Hartooni N., Newman D.K., Johnson A.D. Anaerobic bacteria grow within Candida albicans biofilms and induce biofilm formation in suspension cultures. Curr. Biol. 2014;24:2411–2416. doi: 10.1016/j.cub.2014.08.057.
    1. van Leeuwen P.T., van der Peet J.M., Bikker F.J., Hoogenkamp M.A., Oliveira Paiva A.M., Kostidis S., Mayboroda O.A., Smits W.K., Krom B.P. Interspecies Interactions between Clostridium difficile and Candida albicans. Msphere. 2016;1:e00187-16. doi: 10.1128/mSphere.00187-16.
    1. Somerville G.A., Proctor R.A. Cultivation conditions and the diffusion of oxygen into culture media: the rationale for the flask-to-medium ratio in microbiology. BMC Microbiol. 2013;13:1471–2180. doi: 10.1186/1471-2180-13-9.
    1. Dione N., Khelaifia S., Lagier J.C., Raoult D. The aerobic activity of metronidazole against anaerobic bacteria. Int. J. Antimicrob. Agents. 2015;45:537–540. doi: 10.1016/j.ijantimicag.2014.12.032.
    1. Janus M.M., Crielaard W., Volgenant C.M., van der Veen M.H., Brandt B.W., Krom B.P. Candida albicans alters the bacterial microbiome of early in vitro oral biofilms. J. Oral. Microbiol. 2017;9:1270613. doi: 10.1080/20002297.2016.1270613.
    1. Tampakakis E., Peleg A.Y., Mylonakis E. Interaction of Candida albicans with an intestinal pathogen, Salmonella enterica serovar Typhimurium. Eukaryot. Cell. 2009;8:732–737. doi: 10.1128/EC.00016-09.
    1. Kim Y., Mylonakis E. Killing of Candida albicans filaments by Salmonella enterica serovar Typhimurium is mediated by sopB effectors, parts of a type, I.I.I secretion system. Eukaryot. Cell. 2011;10:782–790. doi: 10.1128/EC.00014-11.
    1. Briard B., Mislin G.L.A., Latge J.P., Beauvais A. Interactions between Aspergillus fumigatus and Pulmonary Bacteria: Current State of the Field, New Data, and Future Perspective. J. Fungi (Basel) 2019;5:48. doi: 10.3390/jof5020048.
    1. Sass G., Nazik H., Penner J., Shah H., Ansari S.R., Clemons K.V., Groleau M.C., Dietl A.M., Visca, Haas H., et al. Aspergillus-Pseudomonas interaction, relevant to competition in airways. Med Mycol. 2019;57:S228–S232. doi: 10.1093/mmy/myy087.
    1. Sass G., Nazik H., Penner J., Shah H., Ansari S.R., Clemons K.V., Groleau M.C., Dietl A.M., Visca P., Haas H., et al. Studies of Pseudomonas aeruginosa Mutants Indicate Pyoverdine as the Central Factor in Inhibition of Aspergillus fumigatus Biofilm. J. Bacteriol. 2017;200:e00345-17. doi: 10.1128/JB.00345-17.
    1. Reece E., Doyle S., Greally P., Renwick J., McClean S. Aspergillus fumigatus Inhibits Pseudomonas aeruginosa in Co-culture: Implications of a Mutually Antagonistic Relationship on Virulence and Inflammation in the, C.F. Airway. Front. Microbiol. 2018;9:1205. doi: 10.3389/fmicb.2018.01205.
    1. Mowat E., Rajendran R., Williams C., McCulloch E., Jones B., Lang S., Ramage G. Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol. Lett. 2010;313:96–102. doi: 10.1111/j.1574-6968.2010.02130.x.
    1. Ferreira J.A., Penner J.C., Moss R.B., Haagensen J.A., Clemons K.V., Spormann A.M., Nazik H., Cohen K., Banaei N., Carolino E., et al. Inhibition of Aspergillus fumigatus and Its Biofilm by Pseudomonas aeruginosa Is Dependent on the Source, Phenotype and Growth Conditions of the Bacterium. PLoS ONE. 2015;10:e0134692. doi: 10.1371/journal.pone.0134692.
    1. Sass G., Ansari S.R., Dietl A.M., Deziel E., Haas H., Stevens D.A. Intermicrobial interaction: Aspergillus fumigatus siderophores protect against competition by Pseudomonas aeruginosa. PLoS ONE. 2019;14:e0216085. doi: 10.1371/journal.pone.0216085.
    1. Briard B., Heddergott C., Latge J.P. Volatile Compounds Emitted by Pseudomonas aeruginosa Stimulate Growth of the Fungal Pathogen Aspergillus fumigatus. Mbio. 2016;7:e00219. doi: 10.1128/mBio.00219-16.
    1. Nutzmann H.W., Reyes-Dominguez Y., Scherlach K., Schroeckh V., Horn F., Gacek A., Schümann J., Hertweck C., Strauss J., Brakhage A.A. Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc. Natl. Acad. Sci. USA. 2011;108:14282–14287. doi: 10.1073/pnas.1103523108.
    1. Schroeckh V., Scherlach K., Nutzmann H.W., Shelest E., Schmidt-Heck W., Schuemann J., Martin K., Hertweck C., Brakhage A.A. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA. 2009;106:14558–14563. doi: 10.1073/pnas.0901870106.
    1. Fischer J., Muller S.Y., Netzker T., Jager N., Gacek-Matthews A., Scherlach K., Stroe M.C., García-Altares M., Pezzini F., Schoeler H., et al. Chromatin mapping identifies BasR, a key regulator of bacteria-triggered production of fungal secondary metabolites. Elife. 2018;12:40969. doi: 10.7554/eLife.40969.
    1. Brandl M.T., Carter M.Q., Parker C.T., Chapman M.R., Huynh S., Zhou Y. Salmonella biofilm formation on Aspergillus niger involves cellulose--chitin interactions. PLoS ONE. 2011;6:e25553. doi: 10.1371/journal.pone.0025553.
    1. Nogueira M.F., Pereira L., Jenull S., Kuchler K., Lion T. Klebsiella pneumoniae prevents spore germination and hyphal development of Aspergillus species. Sci. Rep. 2019;9:018–36524. doi: 10.1038/s41598-018-36524-8.
    1. Rella A., Yang M.W., Gruber J., Montagna M.T., Luberto C., Zhang Y.M., Del Poeta M. Pseudomonas aeruginosa inhibits the growth of Cryptococcus species. Mycopathologia. 2012;173:451–461. doi: 10.1007/s11046-011-9494-7.
    1. Teoh-Chan H., Chau P.Y., Ng M.H., Wong P.C. Inhibition of Cryptococcus neoformans by Pseudomonas aeruginosa. J. Med. Microbiol. 1975;8:77–81. doi: 10.1099/00222615-8-1-77.
    1. Frases S., Chaskes S., Dadachova E., Casadevall A. Induction by Klebsiella aerogenes of a melanin-like pigment in Cryptococcus neoformans. Appl. Env. Microbiol. 2006;72:1542–1550. doi: 10.1128/AEM.72.2.1542-1550.2006.
    1. Frases S., Salazar A., Dadachova E., Casadevall A. Cryptococcus neoformans can utilize the bacterial melanin precursor homogentisic acid for fungal melanogenesis. Appl. Env. Microbiol. 2007;73:615–621. doi: 10.1128/AEM.01947-06.
    1. Rick E.M., Woolnough K., Pashley C.H., Wardlaw A.J. Allergic Fungal Airway Disease. J. Investig. Allergol. Clin. Immunol. 2016;26:344–354. doi: 10.18176/jiaci.0122.
    1. Shi Y., Pan C., Wang K., Chen X., Wu X., Chen C.A., Wu B. Synthetic multispecies microbial communities reveals shifts in secondary metabolism and facilitates cryptic natural product discovery. Env. Microbiol. 2017;19:3606–3618. doi: 10.1111/1462-2920.13858.
    1. Butt A.T., Thomas M.S. Iron Acquisition Mechanisms and Their Role in the Virulence of Burkholderia Species. Front. Cell Infect. Microbiol. 2017;7:460. doi: 10.3389/fcimb.2017.00460.
    1. Ross C., Opel V., Scherlach K., Hertweck C. Biosynthesis of antifungal and antibacterial polyketides by Burkholderia gladioli in coculture with Rhizopus microsporus. Mycoses. 2014;3:48–55. doi: 10.1111/myc.12246.
    1. Moebius N., Ross C., Scherlach K., Rohm B., Roth M., Hertweck C. Biosynthesis of the respiratory toxin bongkrekic acid in the pathogenic bacterium Burkholderia gladioli. Chem. Biol. 2012;19:1164–1174. doi: 10.1016/j.chembiol.2012.07.022.
    1. Lackner G., Moebius N., Partida-Martinez L.P., Boland S., Hertweck C. Evolution of an endofungal lifestyle: Deductions from the Burkholderia rhizoxinica genome. BMC Genomics. 2011;12:1471–2164. doi: 10.1186/1471-2164-12-210.
    1. Smith M.G., Des Etages S.G., Snyder M. Microbial synergy via an ethanol-triggered pathway. Mol. Cell Biol. 2004;24:3874–3884. doi: 10.1128/MCB.24.9.3874-3884.2004.
    1. Gandhi J.A., Ekhar V.V., Asplund M.B., Abdulkareem A.F., Ahmadi M., Coelho C., Martinez L.R. Alcohol enhances Acinetobacter baumannii-associated pneumonia and systemic dissemination by impairing neutrophil antimicrobial activity in a murine model of infection. PLoS ONE. 2014;9:e95707. doi: 10.1371/journal.pone.0095707.
    1. Kaur J., Pethani B.P., Kumar S., Kim M., Sunna A., Kautto L., Penesyan A., Paulsen I.T., Nevalainen H. Pseudomonas aeruginosa inhibits the growth of Scedosporium aurantiacum, an opportunistic fungal pathogen isolated from the lungs of cystic fibrosis patients. Front. Microbiol. 2015;6:866. doi: 10.3389/fmicb.2015.00866.
    1. Chen S.C., Patel S., Meyer W., Chapman B., Yu H., Byth K., Middleton P.G., Nevalainen H., Sorrell T.C. Pseudomonas aeruginosa Inhibits the Growth of Scedosporium and Lomentospora In Vitro. Mycopathologia. 2018;183:251–261. doi: 10.1007/s11046-017-0140-x.
    1. Pappas P.G., Lionakis M.S., Arendrup M.C., Ostrosky-Zeichner L., Kullberg B.J. Invasive candidiasis. Nat. Rev. Dis. Primers. 2018;4:18026. doi: 10.1038/nrdp.2018.26.
    1. Chin V.K., Lee T.Y., Rusliza B., Chong P.P. Dissecting Candida albicans Infection from the Perspective of C. albicans Virulence and Omics Approaches on Host-Pathogen Interaction: A Review. Int. J. Mol. Sci. 2016;17:1643. doi: 10.3390/ijms17101643.
    1. Patin E.C., Thompson A., Orr S.J. Pattern recognition receptors in fungal immunity. Semin. Cell Dev. Biol. 2018;8:30541–30544. doi: 10.1016/j.semcdb.2018.03.003.
    1. Espinosa V., Rivera A. Cytokines and the regulation of fungus-specific, C.D.4 T cell differentiation. Cytokine. 2012;58:100–106. doi: 10.1016/j.cyto.2011.11.005.
    1. Pichard D.C., Freeman A.F., Cowen E.W. Primary immunodeficiency update: Part, I.I.. Syndromes associated with mucocutaneous candidiasis and noninfectious cutaneous manifestations. J. Am. Acad. Dermatol. 2015;73:367–381. doi: 10.1016/j.jaad.2015.01.055.
    1. Chaplin D.D. Overview of the immune response. J. Allergy Clin. Immunol. 2010;125:980. doi: 10.1016/j.jaci.2009.12.980.
    1. Lewis M.L., Surewaard B.G.J. Neutrophil evasion strategies by Streptococcus pneumoniae and Staphylococcus aureus. Cell Tissue Res. 2018;371:489–503. doi: 10.1007/s00441-017-2737-2.
    1. Hernandez-Chavez M.J., Perez-Garcia L.A., Nino-Vega G.A., Mora-Montes H.M. Fungal Strategies to Evade the Host Immune Recognition. J. Fungi (Basel) 2017;3:51. doi: 10.3390/jof3040051.
    1. Chow S.H., Deo P., Naderer T. Macrophage cell death in microbial infections. Cell Microbiol. 2016;18:466–474. doi: 10.1111/cmi.12573.
    1. Ricciardi B.F., Muthukrishnan G., Masters E., Ninomiya M., Lee C.C., Schwarz E.M. Staphylococcus aureus Evasion of Host Immunity in the Setting of Prosthetic Joint Infection: Biofilm and Beyond. Curr. Rev. Musculoskelet Med. 2018;9:018–9501. doi: 10.1007/s12178-018-9501-4.
    1. Byndloss M.X., Tsolis R.M. Chronic Bacterial Pathogens: Mechanisms of Persistence. Microbiol. Spectr. 2016;4:0020–2015. doi: 10.1128/microbiolspec.VMBF-0020-2015.
    1. Bernal-Bayard J., Ramos-Morales F. Molecular Mechanisms Used by Salmonella to Evade the Immune System. Curr. Issues Mol. Biol. 2018;25:133–168. doi: 10.21775/cimb.025.133.
    1. Roux D., Gaudry S., Dreyfuss D., El-Benna J., de Prost N., Denamur E., Saumon G., Ricard J.D. Candida albicans impairs macrophage function and facilitates Pseudomonas aeruginosa pneumonia in rat. Crit. Care Med. 2009;37:1062–1067. doi: 10.1097/CCM.0b013e31819629d2.
    1. Xu H., Sobue T., Bertolini M., Thompson A., Vickerman M., Nobile C.J., Dongari-Bagtzoglou A. S. oralis activates the Efg1 filamentation pathway in C. albicans to promote cross-kingdom interactions and mucosal biofilms. Virulence. 2017;8:1602–1617. doi: 10.1080/21505594.2017.1326438.
    1. Nash E.E., Peters B.M., Fidel P.L., Noverr M.C. Morphology-Independent Virulence of Candida Species during Polymicrobial Intra-abdominal Infections with Staphylococcus aureus. Infect. Immun. 2015;84:90–98. doi: 10.1128/IAI.01059-15.
    1. Kean R., Rajendran R., Haggarty J., Townsend E.M., Short B., Burgess K.E., Lang S., Millington O., Mackay W.G., Williams C., et al. Candida albicans Mycofilms Support Staphylococcus aureus Colonization and Enhances Miconazole Resistance in Dual-Species Interactions. Front. Microbiol. 2017;8:258. doi: 10.3389/fmicb.2017.00258.
    1. Holt J.E., Houston A., Adams C., Edwards S., Kjellerup B.V. Role of extracellular polymeric substances in polymicrobial biofilm infections of Staphylococcus epidermidis and Candida albicans modelled in the nematode Caenorhabditis elegans. Pathog Dis. 2017;75 doi: 10.1093/femspd/ftx052.
    1. Ader F., Jawhara S., Nseir S., Kipnis E., Faure K., Vuotto F., Chemani C., Sendid B., Poulain D., Guery B. Short term Candida albicans colonization reduces Pseudomonas aeruginosa-related lung injury and bacterial burden in a murine model. Crit. Care. 2011;15:R150. doi: 10.1186/cc10276.
    1. Lopez-Medina E., Fan D., Coughlin L.A., Ho E.X., Lamont I.L., Reimmann C., Hooper L.V., Koh A.Y. Candida albicans Inhibits Pseudomonas aeruginosa Virulence through Suppression of Pyochelin and Pyoverdine Biosynthesis. Plos Pathog. 2015;11:e1005129. doi: 10.1371/journal.ppat.1005129.
    1. Diaz P.I., Xie Z., Sobue T., Thompson A., Biyikoglu B., Ricker A., Ikonomou L., Dongari-Bagtzoglou A. Synergistic interaction between Candida albicans and commensal oral streptococci in a novel in vitro mucosal model. Infect. Immun. 2012;80:620–632. doi: 10.1128/IAI.05896-11.
    1. Nash E.E., Peters B.M., Palmer G.E., Fidel P.L., Noverr M.C. Morphogenesis is not required for Candida albicans-Staphylococcus aureus intra-abdominal infection-mediated dissemination and lethal sepsis. Infect. Immun. 2014;82:3426–3435. doi: 10.1128/IAI.01746-14.
    1. Ermolaeva M.A., Schumacher B. Insights from the worm: the C. elegans model for innate immunity. Semin. Immunol. 2014;26:303–309. doi: 10.1016/j.smim.2014.04.005.
    1. Fehrmann C., Jurk K., Bertling A., Seidel G., Fegeler W., Kehrel B.E., Peters G., Becker K., Heilmann C. Role for the fibrinogen-binding proteins coagulase and Efb in the Staphylococcus aureus-Candida interaction. Int. J. Med. Microbiol. 2013;303:230–238. doi: 10.1016/j.ijmm.2013.02.011.
    1. Villena J., Salva S., Aguero G., Alvarez S. Immunomodulatory and protective effect of probiotic Lactobacillus casei against Candida albicans infection in malnourished mice. Microbiol. Immunol. 2011;55:434–445. doi: 10.1111/j.1348-0421.2011.00334.x.
    1. Zelante T., Iannitti R.G., Cunha C., De Luca A., Giovannini G., Pieraccini G., Zecchi R., D’Angelo C., Massi-Benedetti C., Fallarino F., et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 2013;39:372–385. doi: 10.1016/j.immuni.2013.08.003.
    1. Bork P., Beckmann G. The, C.U.B domain. A widespread module in developmentally regulated proteins. J. Mol. Biol. 1993;231:539–545. doi: 10.1006/jmbi.1993.1305.
    1. Arvanitis M., Mylonakis E. Characteristics, Clinical Relevance, and the Role of Echinocandins in Fungal-Bacterial Interactions. Clin. Infect. Dis. 2015;61:S630–634. doi: 10.1093/cid/civ816.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren