Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans
Open accessAbstract
The Gram-positive bacterium Enterococcus faecalis and the fungus Candida albicans are both found as commensals in many of the same niches of the human body, such as the oral cavity and gastrointestinal (GI) tract. However, both are opportunistic pathogens and have frequently been found to be coconstituents of polymicrobial infections. Despite these features in common, there has been little investigation into whether these microbes affect one another in a biologically significant manner. Using a Caenorhabditis elegans model of polymicrobial infection, we discovered that E. faecalis and C. albicans negatively impact each other's virulence. Much of the negative effect of E. faecalis on C. albicans was due to the inhibition of C. albicans hyphal morphogenesis, a developmental program crucial to C. albicans pathogenicity. We discovered that the inhibition was partially dependent on the Fsr quorum-sensing system, a major regulator of virulence in E. faecalis . Specifically, two proteases regulated by Fsr, GelE and SerE, were partially required. Further characterization of the inhibitory signal revealed that it is secreted into the supernatant, is heat resistant, and is between 3 and 10 kDa. The substance was also shown to inhibit C. albicans filamentation in the context of an in vitro biofilm. Finally, a screen of an E. faecalis transposon mutant library identified other genes required for suppression of C. albicans hyphal formation. Overall, we demonstrate a biologically relevant interaction between two clinically important microbes that could affect treatment strategies as well as impact our understanding of interkingdom signaling and sensing in the human-associated microbiome.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Enterococcus faecalis can inhibit C. albicans morphogenesis, biofilm formation, and overall virulence.
“This is exemplified by a series of articles in the last few years by the Lorenz and Garsin groups, who initially reported on the interactions between Enterococcus faecalis and C. albicans, whereby the bacterium can inhibit C. albicans morphogenesis, biofilm formation, and overall virulence [59].”
From Antifungal therapy of Candida biofilms: Past, present and future (2023) · cites this paper as [59]
Candida albicans interacts with several bacterial species found in the gut, such as Enterococcus and Escherichia species; those found in the vagina, such as Lactobacillus species; and those found in the lungs of patients with cystic fibrosis, such as Pseudomonas aeruginosa.
“C. albicans also interacts with several bacterial species found in the gut, such as Enterococcus and Escherichia species; those found in the vagina, such as Lactobacillus species; and those found in the lungs of patients with cystic fibrosis, such as Pseudomonas aeruginosa (13, 34, 54, 78).”
From <i>Candida albicans</i> Biofilms and Human Disease (2015) · cites this paper as [34]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H., Wenzel, R. P., & Edmond, M. B. (2004) · Clinical Infectious Diseases · doi:10.1086/421946 · Cited by 4,496 · see citing works
Sherman, F. (1991) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(91)94004-v · Cited by 4,078 · see citing works
Hidron, A. I., Edwards, J. R., Patel, J., Horan, T. C., Sievert, D. M., Pollock, D. A., Fridkin, S. K., & National Healthcare Safety Network Team and Participating National Healthcare Safety Network Facilities (2008) · Infection Control & Hospital Epidemiology · doi:10.1086/591861 · Cited by 3,724 · see citing works
Isogenic strain construction and gene mapping in Candida albicans.
Fonzi, W. A., & Irwin, M. Y. (1993) · Genetics · doi:10.1093/genetics/134.3.717 · Cited by 1,695 · see citing works
Gillum, A. M., Tsay, E. Y. H., & Kirsch, D. R. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00328721 · Cited by 1,253 · see citing works
Role of Mobile DNA in the Evolution of Vancomycin-Resistant Enterococcus faecalis
Paulsen, I. T., Banerjei, L., Myers, G. S. A., Nelson, W. C., Seshadri, R., Read, T. D., Fouts, D. E., Eisen, J. A., Gill, S. R., Heidelberg, J. F., et al. (2003) · Science · doi:10.1126/science.1080613 · Cited by 930 · see citing works
Overview of manual and automated DNA sequencing by the dideoxy chain termination method
CHEN, E., KUANG, W., & LEE, A. (1991) · Methods · doi:10.1016/s1046-2023(05)80158-6 · Cited by 834 · see citing works
A Recently Evolved Transcriptional Network Controls Biofilm Development in Candida albicans
Nobile, C. J., Fox, E. P., Nett, J. E., Sorrells, T. R., Mitrovich, Q. M., Hernday, A. D., Tuch, B. B., Andes, D. R., & Johnson, A. D. (2012) · Cell · doi:10.1016/j.cell.2011.10.048 · Cited by 711 · see citing works
Brandt, M. E. (2002) · Emerging infectious diseases · doi:10.3201/eid0808.020059 · Cited by 646 · see citing works
Medically important bacterial-fungal interactions
Peleg, A. Y., Hogan, D. A., & Mylonakis, E. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2313 · Cited by 619 · see citing works
Pseudomonas - Candida Interactions: An Ecological Role for Virulence Factors
Hogan, D. A., & Kolter, R. (2002) · Science · doi:10.1126/science.1070784 · Cited by 580 · see citing works
Hogan, D. A., Vik, Å., & Kolter, R. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04349.x · Cited by 575 · see citing works
A simple model host for identifying Gram-positive virulence factors
Garsin, D. A., Sifri, C. D., Mylonakis, E. E., Qin, X., Singh, K. V., Murray, B. E., Calderwood, S. B., & Ausubel, F. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191378698 · Cited by 570 · see citing works
Self-citationHarriott, M. M., & Noverr, M. C. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00657-09 · Cited by 526 · see citing works
Biswas, S., Dijck, P. V., & Datta, A. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00009-06 · Cited by 516 · see citing works
In vitro susceptibility studies of vancomycin-resistant Enterococcus faecalis
Sahm, D. F., Kissinger, J. C., Gilmore, M. S., Murray, P. R., Mulder, R., Solliday, J., & Clarke, B. (1989) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.33.9.1588 · Cited by 497 · see citing works
Our Current Understanding of Fungal Biofilms
Ramage, G., Mowat, E., Jones, B., Williams, C., & Lopez-Ribot, J. (2009) · Critical Reviews in Microbiology · doi:10.3109/10408410903241436 · Cited by 483 · see citing works
Regulation of Cell-Surface Genes and Biofilm Formation by the C. albicans Transcription Factor Bcr1p
Nobile, C. J., & Mitchell, A. P. (2005) · Current Biology · doi:10.1016/j.cub.2005.05.047 · Cited by 464 · see citing works
C. elegans : a practical approach
Hope, I. D. (1999) · Cited by 449 · see citing works
Isolation of yeasts and enteric bacteria in root‐filled teeth with chronic apical periodontitis
Pečiulienė, V., Reynaud, A. H., Balčiūnienė, I., & Haapasalo, M. (2001) · International Endodontic Journal · doi:10.1046/j.1365-2591.2001.00411.x · Cited by 436 · see citing works
Fungal Adenylyl Cyclase Integrates CO2 Sensing with cAMP Signaling and Virulence
Klengel, T., Liang, W., Chaloupka, J., Ruoff, C., Schröppel, K., Naglik, J. R., Eckert, S. E., Mogensen, E. G., Haynes, K., Tuite, M. F., et al. (2005) · Current Biology · doi:10.1016/j.cub.2005.10.040 · Cited by 409 · see citing works
Cross-kingdom interactions:Candida albicansand bacteria
Shirtliff, M. E., Peters, B. M., & Jabra‐Rizk, M. A. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01668.x · Cited by 399 · see citing works
Qin, X., Singh, K. V., Weinstock, G. M., & Murray, B. E. (2000) · Infection and Immunity · doi:10.1128/iai.68.5.2579-2586.2000 · Cited by 364 · see citing works
Antifungal Chemical Compounds Identified Using a C. elegans Pathogenicity Assay
Breger, J. A., Fuchs, B. B., Aperis, G., Moy, T. I., Ausubel, F. M., & Mylonakis, E. E. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030018 · Cited by 334 · see citing works
Role of Antibiotics and Fungal Microbiota in Driving Pulmonary Allergic Responses
Noverr, M. C., Noggle, R. M., Toews, G. B., & Huffnagle, G. B. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.4996-5003.2004 · Cited by 330 · see citing works
Importance of Candida–bacterial polymicrobial biofilms in disease
Harriott, M. M., & Noverr, M. C. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.07.004 · Cited by 315 · see citing works
Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF
Bourgogne, A., Garsin, D. A., Qin, X., Singh, K. V., Sillanpää, J., Yerrapragada, S., Ding, Y., Dugan-Rocha, S., Buhay, C., Shen, H. M., et al. (2008) · Genome biology · doi:10.1186/gb-2008-9-7-r110 · Cited by 299 · see citing works
Self-citationBamford, C. V., d'Mello, A., Nobbs, A. H., Dutton, L. C., Vickerman, M. M., & Jenkinson, H. F. (2009) · Infection and Immunity · doi:10.1128/iai.00438-09 · Cited by 291 · see citing works
Identification of novel antimicrobials using a live-animal infection model
Moy, T. I., Ball, A. R., Anklesaria, Z., Casadei, G., Lewis, K., & Ausubel, F. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604055103 · Cited by 289 · see citing works
Peters, B. M., Jabra‐Rizk, M. A., Scheper, M. A., Leid, J. G., Costerton, J. W., & Shirtliff, M. E. (2010) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00710.x · Cited by 288 · see citing works
Noverr, M. C., Falkowski, N. R., McDonald, R. A., McKenzie, A. N. J., & Huffnagle, G. B. (2004) · Infection and Immunity · doi:10.1128/iai.73.1.30-38.2005 · Cited by 279 · see citing works
Azoulay, É., Timsit, J., Tafflet, M., de Lassence, A., Darmon, M., Zahar, J., Adrie, C., Garrouste-Orgeas, M., Cohen, Y., Mourvillier, B., et al. (2006) · CHEST Journal · doi:10.1378/chest.129.1.110 · Cited by 272 · see citing works
Bacterial and fungal infections after liver transplantation: An analysis of 284 patients
Wade, J. J., Rolando, N., Hayllar, K. M., Philpott‐Howard, J., Casewell, M. W., & Williams, R. L. (1995) · Hepatology · doi:10.1002/hep.1840210517 · Cited by 271 · see citing works
Candida albicans Interactions with Bacteria in the Context of Human Health and Disease
Morales, D. K., & Hogan, D. A. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000886 · Cited by 270 · see citing works
Nakayama, J., Cao, Y. H., Horii, T., Sakuda, S., Akkermans, A. D. L., de Vos, W. M., & Nagasawa, H. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02486.x · Cited by 263 · see citing works
Qin, X., Singh, K. V., Weinstock, G. M., & Murray, B. E. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.11.3372-3382.2001 · Cited by 251 · see citing works
Davis‐Hanna, A., Piispanen, A. E., Stateva, L. I., & Hogan, D. A. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06013.x · Cited by 249 · see citing works
van der Hoeven, R., McCallum, K. C., Cruz, M. R., & Garsin, D. A. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002453 · Cited by 240 · see citing works
Self-citationCoevolution of Morphology and Virulence in Candida Species
Childers, D. S., Carlisle, P. L., & Kadosh, D. (2011) · Eukaryotic Cell · doi:10.1128/ec.05085-11 · Cited by 227 · see citing works
Sifri, C. D., Mylonakis, E. E., Singh, K. V., Qin, X., Garsin, D. A., Murray, B. E., Ausubel, F. M., & Calderwood, S. B. (2002) · Infection and Immunity · doi:10.1128/iai.70.10.5647-5650.2002 · Cited by 222 · see citing works
Self-citationGeneration and Testing of Mutants ofEnterococcus faecalisin a Mouse Peritonitis Model
Singh, K. V., Qin, X., Weinstock, G. M., & Murray, B. E. (1998) · The Journal of Infectious Diseases · doi:10.1086/314453 · Cited by 208 · see citing works
Murray, B. E., Singh, K. V., Ross, R. P., Heath, J. D., Dunny, G. M., & Weinstock, G. M. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.16.5216-5223.1993 · Cited by 203 · see citing works
Shelburne, S. A., Keith, D. B., Horstmann, N., Sumby, P., Davenport, M. T., Graviss, E. A., Brennan, R. G., & Musser, J. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711767105 · Cited by 194 · see citing works
Models of Caenorhabditis elegans Infection by Bacterial and Fungal Pathogens
Powell, J. R., & Ausubel, F. M. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-570-1_24 · Cited by 192 · see citing works
Pukkila-Worley, R., Peleg, A. Y., Tampakakis, E., & Mylonakis, E. E. (2009) · Eukaryotic Cell · doi:10.1128/ec.00163-09 · Cited by 192 · see citing works
Prokaryote–eukaryote interactions identified by using Caenorhabditis elegans
Peleg, A. Y., Tampakakis, E., Fuchs, B. B., Eliopoulos, G. M., Moellering, R. C., & Mylonakis, E. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805048105 · Cited by 188 · see citing works
Jarosz, L. M., Deng, D. M., van der Mei, H. C., Crielaard, W., & Krom, B. P. (2009) · Eukaryotic Cell · doi:10.1128/ec.00070-09 · Cited by 187 · see citing works
Self-Regulation of Candida albicans Population Size during GI Colonization
White, S. J., Rosenbach, A., Lephart, P., Nguyen, D. T., Benjamin, A., Tzipori, S. R., Whiteway, M. S., Mecsas, J. C., & Kumamoto, C. A. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030184 · Cited by 181 · see citing works
Singh, K. V., Coque, T. M., Weinstock, G. M., & Murray, B. E. (1998) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.1998.tb01180.x · Cited by 179 · see citing works
Mylonakis, E. E., Casadevall, A., & Ausubel, F. M. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030101 · Cited by 175 · see citing works
Summers, K. L., Erb‐Downward, J. R., Falkowski, N. R., Young, V. B., Kao, J. Y., & Huffnagle, G. B. (2011) · Infection and Immunity · doi:10.1128/iai.05162-11 · Cited by 151 · see citing works
Bourgogne, A., Hilsenbeck, S. G., Dunny, G. M., & Murray, B. E. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.8.2875-2884.2006 · Cited by 136 · see citing works
(2002) · ASM Press eBooks · doi:10.1128/9781555817923 · Cited by 132 · see citing works
CO2 Acts as a Signalling Molecule in Populations of the Fungal Pathogen Candida albicans
Hall, R. A., De Sordi, L., MacCallum, D. M., Topal, H., Eaton, R., Bloor, J. W., Robinson, G. K., Levin, L. R., Buck, J., Wang, Y., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001193 · Cited by 126 · see citing works
(1999) · doi:10.1093/oso/9780199637393.001.0001 · Cited by 126 · see citing works
GFP as a quantitative reporter of gene regulation in Candida albicans
Barelle, C. J., Manson, C. L., MacCallum, D. M., Odds, F. C., Gow, N. A. R., & Brown, A. J. P. (2004) · Yeast · doi:10.1002/yea.1099 · Cited by 122 · see citing works
Keppler‐Ross, S., Noffz, C. S., & Dean, N. (2008) · Genetics · doi:10.1534/genetics.108.087080 · Cited by 121 · see citing works
O'Sullivan, J. M., Jenkinson, H. F., & Cannon, R. D. (2000) · Microbiology · doi:10.1099/00221287-146-1-41 · Cited by 109 · see citing works
Ethanolamine Activates a Sensor Histidine Kinase Regulating Its Utilization in Enterococcus faecalis
Papa, M. F. D., & Perego, M. (2008) · Journal of Bacteriology · doi:10.1128/jb.00952-08 · Cited by 84 · see citing works
Interaction of Candida albicans with an Intestinal Pathogen, Salmonella enterica Serovar Typhimurium
Tampakakis, E., Peleg, A. Y., & Mylonakis, E. E. (2009) · Eukaryotic Cell · doi:10.1128/ec.00016-09 · Cited by 84 · see citing works
Neely, A. N., LAW, E. J., & Holder, I. A. (1986) · Infection and Immunity · doi:10.1128/iai.52.1.200-204.1986 · Cited by 73 · see citing works
Garsin, D. A., Urbach, J. M., Huguet‐Tapia, J. C., Peters, J. E., & Ausubel, F. M. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.21.7280-7289.2004 · Cited by 62 · see citing works
Self-citationBiochemical characterization of an anti-Candida factor produced by Enterococcus faecalis
Shekh, M. R., & Roy, U. (2012) · BMC Microbiology · doi:10.1186/1471-2180-12-132 · Cited by 37 · see citing works
Development of a genomic site for gene integration and expression in Enterococcus faecalis
DebRoy, S., van der Hoeven, R., Singh, K. V., Gao, P., Harvey, B. R., Murray, B. E., & Garsin, D. A. (2012) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2012.04.011 · Cited by 36 · see citing works
Self-citationPeptide Signals Sense and Destroy Target Cells
Garsin, D. A. (2004) · Science · doi:10.1126/science.1107236 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [34]34. Garsin DA, Urbach J, Huguet-Tapia JC, Peters JE, Ausubel FM. 2004. Construction of an Enterococcus faecalis Tn917-mediated-gene-disruption library offers insight into Tn917 insertion patterns. J. Bacteriol. 186:7280–7289 [DOI] [PMC free article] [PubMed] [Google Scholar]
Cited by
Sorted by citations
<i>Candida albicans</i> Biofilms and Human Disease
Nobile, C. J., & Johnson, A. D. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104330 · Cited by 1,057 · see citing works
Candida albicans biofilms: development, regulation, and molecular mechanisms
Gulati, M., & Nobile, C. J. (2016) · Microbes and Infection · doi:10.1016/j.micinf.2016.01.002 · Cited by 738 · see citing works
Biofilm-associated infection by enterococci
Ch’ng, J.-H., Chong, K. K. L., Lam, L. N., Wong, J. J., & Kline, K. A. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0107-z · Cited by 449 · see citing works
Richard, M. L., & Sokol, H. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0121-2 · Cited by 414 · see citing works
Rosmarinus officinalis L. (rosemary) as therapeutic and prophylactic agent
de Oliveira, J. R., Camargo, S. E. A., & de Oliveira, L. D. (2019) · Journal of Biomedical Science · doi:10.1186/s12929-019-0499-8 · Cited by 385 · see citing works
Zaborin, A., Smith, D., Garfield, K., Quensen, J., Shakhsheer, B., Kade, M., Tirrell, M., Tiedje, J., Gilbert, J. A., Zaborina, O., et al. (2014) · mBio · doi:10.1128/mbio.01361-14 · Cited by 367 · see citing works
d’Enfert, C., Kaune, A.-K., Alaban, L. R., Chakraborty, S., Cole, N. L., Delavy, M., Kosmala, D., Marsaux, B., Fróis-Martins, R., Morelli, M., et al. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa060 · Cited by 351 · see citing works
Microbiology of the built environment
Gilbert, J. A., & Stephens, B. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0065-5 · Cited by 324 · see citing works
Oxidative Stress Responses in the Human Fungal Pathogen, Candida albicans
Dantas, A., Day, A., Ikeh, M., Kos, I., Achan, B., & Quinn, J. (2015) · Biomolecules · doi:10.3390/biom5010142 · Cited by 281 · see citing works
Graham, C. E., Cruz, M. R., Garsin, D. A., & Lorenz, M. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620432114 · Cited by 239 · see citing works
Self-citationFungal-Bacterial Interactions in Health and Disease
Krüger, W., Vielreicher, S., Kapitan, M., Jacobsen, I. D., & Niemiec, M. J. (2019) · Pathogens · doi:10.3390/pathogens8020070 · Cited by 228 · see citing works
Rapid evolution of microbe-mediated protection against pathogens in a worm host
King, K. C., Brockhurst, M. A., Vasieva, O., Paterson, S., Betts, A., Ford, S. A., Frost, C. L., Horsburgh, M. J., Haldenby, S. T., & Hurst, G. D. D. (2016) · The ISME Journal · doi:10.1038/ismej.2015.259 · Cited by 218 · see citing works
The Fungal Mycobiome and Its Interaction with Gut Bacteria in the Host
Sam, Q. H., Chang, M. W., & Chai, L. Y. A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18020330 · Cited by 211 · see citing works
Mycobiota in gastrointestinal diseases
Mukherjee, P. K., Sendid, B., Hoarau, G., Colombel, J., Poulain, D., & Ghannoum, M. A. (2014) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2014.188 · Cited by 211 · see citing works
Polke, M., Hube, B., & Jacobsen, I. D. (2015) · Advances in applied microbiology · doi:10.1016/bs.aambs.2014.12.002 · Cited by 188 · see citing works
Candida albicans and Candida glabrata : global priority pathogens
Katsipoulaki, M., Stappers, M. H. T., Malavia, D., Brunke, S., Hube, B., & Gow, N. A. R. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00021-23 · Cited by 174 · see citing works
Cross-Domain and Viral Interactions in the Microbiome
Rowan-Nash, A. D., Korry, B. J., Mylonakis, E. E., & Belenky, P. A. (2019) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00044-18 · Cited by 164 · see citing works
Biofilm Models of Polymicrobial Infection
Gabrilska, R. A., & Rumbaugh, K. P. (2015) · Future Microbiology · doi:10.2217/fmb.15.109 · Cited by 152 · see citing works
Role of quorum sensing and chemical communication in fungal biotechnology and pathogenesis
Barriuso, J., Hogan, D. A., Keshavarz, T., & Martı́nez, M. J. (2018) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy022 · Cited by 132 · see citing works
Model systems for the study of Enterococcal colonization and infection
Goh, H. M. S., Yong, A. M. H., Chong, K. K. L., & Kline, K. A. (2017) · Virulence · doi:10.1080/21505594.2017.1279766 · Cited by 131 · see citing works
Caenorhabditis elegans: a model to understand host–microbe interactions
Kumar, A., Baruah, A., Tomioka, M., Iino, Y., Kalita, M. C., & Khan, M. R. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03319-7 · Cited by 118 · see citing works
Candida –Bacteria Interactions: Their Impact on Human Disease
Allison, D. L., Willems, H. M. E., Jayatilake, J. A. M. S., Bruno, V. M., Peters, B. M., & Shirtliff, M. E. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0030-2016 · Cited by 115 · see citing works
Invertebrate models of fungal infection
Arvanitis, M., Glavis‐Bloom, J., & Mylonakis, E. E. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.03.008 · Cited by 112 · see citing works
MacAlpine, J., Daniel-Ivad, M., Liu, Z., Yano, J., Revie, N. M., Todd, R. T., Stogios, P. J., Sánchez, H., O’Meara, T. R., Tompkins, T. A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26390-w · Cited by 111 · see citing works
Zeise, K. D., Woods, R. J., & Huffnagle, G. B. (2021) · Clinical Microbiology Reviews · doi:10.1128/cmr.00323-20 · Cited by 101 · see citing works
PolymicrobialCandidabiofilms: friends and foe in the oral cavity
O’Donnell, L. E., Millhouse, E., Sherry, L., Kean, R., Malcolm, J., Nile, C. J., & Ramage, G. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov077 · Cited by 102 · see citing works
Commensals, probiotics and pathogens in the C aenorhabditis elegans model
Clark, L. C., & Hodgkin, J. (2013) · Cellular Microbiology · doi:10.1111/cmi.12234 · Cited by 101 · see citing works
Fungi as Part of the Microbiota and Interactions with Intestinal Bacteria
Kapitan, M., Niemiec, M. J., Steimle, A., Frick, J.-S., & Jacobsen, I. D. (2018) · Current topics in microbiology and immunology · doi:10.1007/82_2018_117 · Cited by 93 · see citing works
The mammalian mycobiome: A complex system in a dynamic relationship with the host
Lai, G. C., Tan, T. G., & Pavelka, N. (2018) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1438 · Cited by 91 · see citing works
Candida Interactions with the Oral Bacterial Microbiota
Montelongo‐Jauregui, D., & Lopez-Ribot, J. L. (2018) · Journal of Fungi · doi:10.3390/jof4040122 · Cited by 93 · see citing works
Polymicrobial Interactions in the Urinary Tract: Is the Enemy of My Enemy My Friend?
Gaston, J. R., Johnson, A. O., Bair, K. L., White, A. N., & Armbruster, C. E. (2021) · Infection and Immunity · doi:10.1128/iai.00652-20 · Cited by 90 · see citing works
Romo, J. A., & Kumamoto, C. A. (2020) · Journal of Fungi · doi:10.3390/jof6010016 · Cited by 97 · see citing works
Streptococcus gordonii comCDE (competence) operon modulates biofilm formation with Candida albicans
Jack, A. A., Daniels, D. E., Jepson, M. A., Vickerman, M. M., Lamont, R. J., Jenkinson, H. F., & Nobbs, A. H. (2015) · Microbiology · doi:10.1099/mic.0.000010 · Cited by 88 · see citing works
de Oliveira, J. R., de Jesus, D., Figueira, L. W., de Oliveira, F. E., Soares, C. P., Camargo, S. E. A., Jorge, A. O. C., & de Oliveira, L. D. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370216688571 · Cited by 85 · see citing works
Graf, K., Last, A., Gratz, R., Allert, S., Linde, S., Westermann, M., Gröger, M., Mosig, A. S., Gresnigt, M. S., & Hube, B. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.039719 · Cited by 83 · see citing works
Bor, B., Cen, L., Agnello, M., Shi, W., & He, X. (2016) · Scientific Reports · doi:10.1038/srep27956 · Cited by 81 · see citing works
Chemical Mediators at the Bacterial-Fungal Interface
Scherlach, K., & Hertweck, C. (2020) · Annual Review of Microbiology · doi:10.1146/annurev-micro-012420-081224 · Cited by 81 · see citing works
Caenorhabditis elegans, a Host to Investigate the Probiotic Properties of Beneficial Microorganisms
Poupet, C., Chassard, C., Nivoliez, A., & Bornes, S. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.00135 · Cited by 81 · see citing works
Quorum-Sensing Regulation of Virulence Factors in Bacterial Biofilm
Warrier, A., Satyamoorthy, K., & Murali, T. S. (2021) · Future Microbiology · doi:10.2217/fmb-2020-0301 · Cited by 77 · see citing works
Intercellular communications in multispecies oral microbial communities
Guo, L., He, X., & Shi, W. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00328 · Cited by 77 · see citing works
The interplay between gut bacteria and the yeast Candida albicans
Pérez, J. C. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1979877 · Cited by 74 · see citing works
Dixon, E. F., & Hall, R. A. (2015) · Cellular Microbiology · doi:10.1111/cmi.12490 · Cited by 73 · see citing works
Dressed to impress: impact of environmental adaptation on the C andida albicans cell wall
Hall, R. A. (2015) · Molecular Microbiology · doi:10.1111/mmi.13020 · Cited by 73 · see citing works
Gow, N. A. R., & Netea, M. G. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0462 · Cited by 75 · see citing works
Haque, S., Yadav, D. K., Bisht, S. C., Yadav, N., Singh, V., Dubey, K. K., Jawed, A., Wahid, M., & Dar, S. A. (2019) · Journal of Chemotherapy · doi:10.1080/1120009x.2019.1599175 · Cited by 69 · see citing works
Bacterial‐fungal interactions and their impact on microbial pathogenesis
MacAlpine, J., Robbins, N., & Cowen, L. E. (2022) · Molecular Ecology · doi:10.1111/mec.16411 · Cited by 72 · see citing works
Yuen, G. J., & Ausubel, F. M. (2018) · Virulence · doi:10.1080/21505594.2018.1438025 · Cited by 67 · see citing works
Enemies and brothers in arms:Candida albicansand gram-positive bacteria
Förster, T. M., Mogavero, S., Dräger, A., Graf, K., Polke, M., Jacobsen, I. D., & Hube, B. (2016) · Cellular Microbiology · doi:10.1111/cmi.12657 · Cited by 65 · see citing works
Commensal fungi in intestinal health and disease
Ost, K. S., & Round, J. L. (2023) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00816-w · Cited by 65 · see citing works
Manganyi, M. C., Regnier, T. J. C., & Olivier, E. I. (2015) · South African Journal of Botany · doi:10.1016/j.sajb.2015.03.192 · Cited by 63 · see citing works
Candida albicansandEnterococcus faecalisin the gut
Garsin, D. A., & Lorenz, M. C. (2013) · Gut Microbes · doi:10.4161/gmic.26040 · Cited by 60 · see citing works
Self-citationElashiry, M. M., Bergeron, B. E., & Tay, F. R. (2023) · Microbial Pathogenesis · doi:10.1016/j.micpath.2023.106337 · Cited by 63 · see citing works
The Relationship of Candida albicans with the Oral Bacterial Microbiome in Health and Disease
Bertolini, M., & Dongari‐Bagtzoglou, A. I. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-28524-1_6 · Cited by 61 · see citing works
Mixed biofilms of pathogenic Candida-bacteria: regulation mechanisms and treatment strategies
Khan, F., Bamunuarachchi, N. I., Pham, D. T. N., Tabassum, N., Khan, M. S., & Kim, Y. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2021.1921696 · Cited by 61 · see citing works
Host’s Immunity and Candida Species Associated with Denture Stomatitis: A Narrative Review
Bars, P. L., Kouadio, A. A., Bandiaky, O. N., Guéhennec, L. L., & de la Cochetière, M.-F. (2022) · Microorganisms · doi:10.3390/microorganisms10071437 · Cited by 68 · see citing works
Pathogenetic Impact of Bacterial–Fungal Interactions
Nogueira, F., Sharghi, S., Kuchler, K., & Lion, T. (2019) · Microorganisms · doi:10.3390/microorganisms7100459 · Cited by 57 · see citing works
Caenorhabditis elegans in high-throughput screens for anti-infective compounds
Peterson, N., & Pukkila-Worley, R. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.06.003 · Cited by 53 · see citing works
Antifungal therapy of Candida biofilms: Past, present and future
Ajetunmobi, O. H., Badali, H., Romo, J. A., Ramage, G., & Lopez-Ribot, J. L. (2023) · Biofilm · doi:10.1016/j.bioflm.2023.100126 · Cited by 52 · see citing works
Caenorhabditis elegans as a Model Host to Monitor the Candida Infection Processes
Elkabti, A. B., Issi, L., & Rao, R. P. (2018) · Journal of Fungi · doi:10.3390/jof4040123 · Cited by 51 · see citing works
Klebsiella pneumoniae prevents spore germination and hyphal development of Aspergillus species
Nogueira, F., Pereira, L., Jenull, S., Kuchler, K., & Lion, T. (2019) · Scientific Reports · doi:10.1038/s41598-018-36524-8 · Cited by 50 · see citing works
Brown, A. O., Graham, C. E., Cruz, M. R., Singh, K. V., Murray, B. E., Lorenz, M. C., & Garsin, D. A. (2019) · mBio · doi:10.1128/mbio.01334-19 · Cited by 46 · see citing works
Self-citationCandida albicans morphology: still in focus
Jacobsen, I. D., & Hube, B. (2017) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2017.1290524 · Cited by 45 · see citing works
van der Hoeven, R., Cruz, M. R., Chávez, V., & Garsin, D. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124091 · Cited by 43 · see citing works
Self-citationInhibition of mixed fungal and bacterial biofilms on silicone by carboxymethyl chitosan
Tan, Y., Leonhard, M., Moser, D., Ma, S., & Schneider‐Stickler, B. (2016) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2016.08.061 · Cited by 43 · see citing works
Candida–Bacterial Biofilms and Host–Microbe Interactions in Oral Diseases
Negrini, T. D. C., Koo, H., & Arthur, R. A. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-28524-1_10 · Cited by 44 · see citing works
Sensing of the Microbial Neighborhood by Candida albicans
Mallick, E. M., & Bennett, R. J. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003661 · Cited by 42 · see citing works
Kousser, C., Clark, C., Sherrington, S. L., Voelz, K., & Hall, R. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-42175-0 · Cited by 40 · see citing works
Tan, Y., Leonhard, M., Moser, D., & Schneider‐Stickler, B. (2017) · Microbial Pathogenesis · doi:10.1016/j.micpath.2017.10.051 · Cited by 39 · see citing works
Nazari-Vanani, R., Sattarahmady, N., Yadegari, H., & Heli, H. (2018) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2018.03.025 · Cited by 38 · see citing works
Krishnamoorthy, A. L., Lemus, A. A., Solomon, A. P., Valm, A. M., & Neelakantan, P. (2020) · Microorganisms · doi:10.3390/microorganisms8111771 · Cited by 37 · see citing works
Anti-Candida albicans biofilm effect of novel heterocyclic compounds
Kagan, S. A., Jabbour, A. R., Sionov, E., Al-Quntar, A., Steinberg, D., Srebnik, M., Nir‐Paz, R., Weiss, A. M., & Polacheck, I. (2013) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkt365 · Cited by 37 · see citing works
Fei, W., Wang, Z., & Tang, J. (2023) · Gut Pathogens · doi:10.1186/s13099-023-00559-8 · Cited by 34 · see citing works
Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms.
Demuyser, L., Jabra-Rizk, M., & van Dijck, P. (2014) · Pathogens and Disease · doi:10.1111/2049-632x.12123 · Cited by 37 · see citing works
Quorum sensing mechanisms in fungi
Barriuso, J., & Centro de Investigaciones Biológicas, C. S. D. I. C. (2015) · AIMS Microbiology · doi:10.3934/microbiol.2015.1.37 · Cited by 35 · see citing works
Yu, X., Fu, F., Kong, W.-N., Xuan, Q., Wen, D., Chen, X., Yong-ming, H., He, L.-H., Guo, J., Zhou, A.-P., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00198 · Cited by 35 · see citing works
Fungi at the Scene of the Crime: Innocent Bystanders or Accomplices in Oral Infections?
Delaney, C., Kean, R., Short, B., Tumelty, M., McLean, W., Nile, C. J., & Ramage, G. (2018) · Current Clinical Microbiology Reports · doi:10.1007/s40588-018-0100-3 · Cited by 33 · see citing works
Co‐ and polymicrobial infections in the gut mucosa: The host–microbiota–pathogen perspective
Frisan, T. (2020) · Cellular Microbiology · doi:10.1111/cmi.13279 · Cited by 33 · see citing works
Lordello, V. B., Meneguin, A. B., de Annunzio, S. R., Taranto, M. P., Chorilli, M., Fontana, C. R., & Cavallini, D. C. U. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13070998 · Cited by 32 · see citing works
Symbiosis and Dysbiosis of the Human Mycobiome
Mishra, K., Bukavina, L., & Ghannoum, M. A. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.636131 · Cited by 32 · see citing works
Cruz, M. R., Cristy, S., Guha, S., De Cesare, G. B., Evdokimova, E., Sanchez, H., Borek, D., Miramón, P., Yano, J., Fidel, P. L., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33613-1 · Cited by 30 · see citing works
Self-citationFungi in the Gut Microbiota: Interactions, Homeostasis, and Host Physiology
Liu, H., Li, S., Ogamune, K. J., Ahmed, A. A., Kim, I. H., Zhang, Y., & Cai, D. (2025) · Microorganisms · doi:10.3390/microorganisms13010070 · Cited by 34 · see citing works
Kart, D., Ciftci, S. Y., & Nemutlu, E. (2019) · Microbiological Research · doi:10.1016/j.micres.2019.126346 · Cited by 32 · see citing works
Bender, J. M., Li, F., Purswani, H., Capretz, T., Cerini, C., Zabih, S., Hung, L. T., Francis, N., Chin, S., Pannaraj, P. S., et al. (2019) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2019.1684466 · Cited by 31 · see citing works
Tartor, Y. H., Elmowalid, G. A., Hassan, M. N., Shaker, A., Ashour, D. F., & Saber, T. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.807218 · Cited by 30 · see citing works
Inhibition of Candida albicans biofilm development by unencapsulated Enterococcus faecalis cps2
Bachtiar, E. W., Dewiyani, S., Akbar, S. M. S., & Bachtiar, B. M. (2016) · Journal of Dental Sciences · doi:10.1016/j.jds.2016.03.012 · Cited by 29 · see citing works
Candida albicans and Enterococcus faecalis biofilm frenemies: When the relationship sours
Alshanta, O. A., Albashaireh, K. Z., McKloud, E., Delaney, C., Kean, R., McLean, W., & Ramage, G. (2022) · Biofilm · doi:10.1016/j.bioflm.2022.100072 · Cited by 29 · see citing works
Future therapies targeted towards eliminatingCandidabiofilms and associated infections
Bandara, N., Matsubara, V. H., & Samaranayake, L. P. (2016) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2017.1268530 · Cited by 29 · see citing works
Intestinal bacteria—a powerful weapon for fungal infections treatment
Cong, L., Chen, C., Mao, S., Han, Z., Zhu, Z., & Li, Y. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1187831 · Cited by 29 · see citing works
Tiller, G. R., & Garsin, D. A. (2014) · Genetics · doi:10.1534/genetics.113.160606 · Cited by 26 · see citing works
Self-citationPseudogymnoascus destructans growth in wood, soil and guano substrates
Urbina, J. C., Chestnut, T., Allen, J. M., & Levi, T. (2021) · Scientific Reports · doi:10.1038/s41598-020-80707-1 · Cited by 25 · see citing works
LeValley, S. L., Tomaro-Duchesneau, C., & Britton, R. A. (2020) · mSphere · doi:10.1128/msphere.00585-19 · Cited by 25 · see citing works
The potential influence of two Enterococcus faecium on the growth of Listeria monocytogenes
Huang, Y., Ye, K., Yu, K., Wang, K., & Zhou, G. (2016) · Food Control · doi:10.1016/j.foodcont.2016.02.009 · Cited by 24 · see citing works
West, P. T., Peters, S. L., Olm, M. R., Yu, F. B., Gause, H., Lou, Y. C., Firek, B., Baker, R. W., Johnson, A. D., Morowitz, M. J., et al. (2021) · Microbiome · doi:10.1186/s40168-021-01085-y · Cited by 25 · see citing works
Interactions between invasive fungi and symbiotic bacteria
Wang, F., Xin, C., Liu, J., Ran, Z., Zhao, C., & Song, Z. (2020) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-020-02913-3 · Cited by 22 · see citing works
Hameed, S., Hans, S., Monasky, R. C., Thangamani, S., & Fatima, Z. (2021) · Pathogens · doi:10.3390/pathogens10020183 · Cited by 23 · see citing works
Willett, J. L. E., & Dunny, G. M. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00081-23 · Cited by 22 · see citing works
The role of gut microbiota in infectious diseases
Cai, Y., Chen, L., Zhang, S., Zeng, L., & Zeng, G. (2022) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1551 · Cited by 18 · see citing works
Tomé, F. M., Ramos, L. D. P., Freire, F., Pereira, C. A., de Oliveira, I. C. B., Junqueira, J. C., Jorge, A. O. C., & de Oliveira, L. D. (2017) · Lasers in Medical Science · doi:10.1007/s10103-017-2201-2 · Cited by 18 · see citing works
Tipping the Balance: C. albicans Adaptation in Polymicrobial Environments
Ranjan, A. K., & Dongari‐Bagtzoglou, A. I. (2018) · Journal of Fungi · doi:10.3390/jof4030112 · Cited by 18 · see citing works
Heme peroxidase HPX-2 protects Caenorhabditis elegans from pathogens
Liu, Y., Kaval, K. G., van Hoof, A., & Garsin, D. A. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1007944 · Cited by 17 · see citing works
Self-citation
- Authors
- Cruz, M. R., Graham, C. E., Gagliano, B. C., Lorenz, M. C., & Garsin, D. A.
- Affiliations
- The University of Texas Health Science Center at Houston (US)
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2013-01
- Volume
- 81
- Issue
- 1
- Pages
- 189-200
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC3536143
- OpenAlex
- W2165496886
- Cited by
- 188
- References
- 65
- Citations by year
- 2026: 12 · 2025: 14 · 2024: 8 · 2023: 10 · 2022: 14 · 2021: 26 · 2020: 16 · 2019: 19 · 2018: 16 · 2017: 11 · 2016: 12 · 2015: 14 · 2014: 9 · 2013: 7
- FWCI
- 6.63
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Infection and Immunity (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Texas Health Science Center at Houston
- National Institute of Allergy and Infectious Diseases (R01AI075091, R01AI076406, R56AI093699)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- Enterococcus faecalis, Candida albicans, hyphal morphogenesis, fungal virulence, co-infection, interkingdom signaling, Caenorhabditis elegans model, biofilm, transposon mutant screen, opportunistic pathogens, human microbiome
- MeSH terms
- Animals, Bacterial Proteins, Candida albicans, Candidiasis, Morphogenesis, Enterococcus faecalis, Virulence, Gram-Positive Bacterial Infections, Caenorhabditis elegans, Biofilms, Hyphae, Quorum Sensing, Coinfection
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review