Bacterial fight-and-flight responses enhance virulence in a polymicrobial infection
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Significance: Polymicrobial synergy occurs when infections caused by more than one species are more severe than the sum of the individual species acting alone. Here, we show that a bacterial fight-and-flight response to an antimicrobial, hydrogen peroxide (H 2 O 2 ), is required for a pathogen to display synergy with a commensal bacterium in vivo. H 2 O 2 is generated by the commensal, and in response, the pathogen either enzymatically destroys (fights) the antimicrobial or disperses away (takes flight) from the antimicrobial-producing commensal. Remarkably, both behaviors are critical for the pathogen to display synergy during coinfection. Moreover, when the pathogen is unable to disperse, the community loses spatial organization, trapping the pathogen next to the commensal.
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When co-cultured with Streptococcus gordonii, Aggregatibacter actinomycetemcomitans cells upregulated the dspB gene encoding the poly-N-acetyl-d-glucosamine-degrading enzyme Dispersin B.
“When co-cultured with S. gordonii, A. actinomycetemcomitans cells upregulated the dspB gene encoding the poly-N-acetyl-d-glucosamine–degrading enzyme Dispersin B.81”
From The dental plaque biofilm matrix (2021) · cites this paper as [81]
The Results report significantly enhanced dspB transcription when Aggregatibacter actinomycetemcomitans was cocultured with Streptococcus gordonii under oxic conditions, and identify dspB as encoding Dispersin B. Our copy calls it a biofilm-dispersing enzyme but does not specify that it degrades poly-N-acetyl-d-glucosamine. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe matrix helps to position cells at a distance where mutually beneficial interactions are optimized and competition is minimized.
“The matrix helps to position cells at a distance where mutually beneficial interactions are optimized and competition is minimized.81,230”
From The dental plaque biofilm matrix (2021) · cites this paper as [81]
The paper reports that DspB breaks down a component of the biofilm matrix and is required for Aggregatibacter actinomycetemcomitans to position itself farther from Streptococcus gordonii (main text; “DspB Modulates Community Spatial Structure in Vivo,” page unavailable). It proposes, rather than demonstrates, that this spacing maximizes access to beneficial lactate while minimizing exposure to inhibitory hydrogen peroxide. The claim presents that proposed optimization as established and generalizes the finding from matrix remodeling to the matrix itself. (LLM, conf=0.82)
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Cites
Bacterial biofilms: from the Natural environment to infectious diseases
Hall‐Stoodley, L., Costerton, J. W., & Stoodley, P. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro821 · Cited by 7,133 · see citing works
Bacterial competition: surviving and thriving in the microbial jungle
Hibbing, M. E., Fuqua, C., Parsek, M. R., & Peterson, S. B. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2259 · Cited by 2,658 · see citing works
Imlay, J. A. (2003) · Annual Review of Microbiology · doi:10.1146/annurev.micro.57.030502.090938 · Cited by 2,206 · see citing works
Periodontitis: a polymicrobial disruption of host homeostasis
Darveau, R. P. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2337 · Cited by 1,688 · see citing works
Oral multispecies biofilm development and the key role of cell–cell distance
Kolenbrander, P. E., Palmer, R. J., Periasamy, S., & Jakubovics, N. S. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2381 · Cited by 1,309 · see citing works
Molecular basis of intercellular adhesion in the biofilm‐forming Staphylococcus epidermidis
Heilmann, C., Schweitzer, O., Gerke, C., Vanittanakom, N., Mack, D., & Götz, F. (1996) · Molecular Microbiology · doi:10.1111/j.1365-2958.1996.tb02548.x · Cited by 912 · see citing works
Polymicrobial Interactions: Impact on Pathogenesis and Human Disease
Peters, B. M., Jabra‐Rizk, M. A., O’May, G. A., Costerton, J. W., & Shirtliff, M. E. (2012) · Clinical Microbiology Reviews · doi:10.1128/cmr.00013-11 · Cited by 713 · see citing works
Bacterial diversity in the oral cavity of 10 healthy individuals
Bik, E. M., Long, C. D., Armitage, G. C., Loomer, P., Emerson, J., Mongodin, E. F., Nelson, K. E., Gill, S. R., Fraser-Liggett, C. M., & Relman, D. A. (2010) · The ISME Journal · doi:10.1038/ismej.2010.30 · Cited by 651 · see citing works
daime , a novel image analysis program for microbial ecology and biofilm research
Daims, H., Lücker, S., & Wagner, M. (2005) · Environmental Microbiology · doi:10.1111/j.1462-2920.2005.00880.x · Cited by 606 · see citing works
Bacterial diversity within the human subgingival crevice
Kroes, I., Lepp, P. W., & Relman, D. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.25.14547 · Cited by 606 · see citing works
Xiao, J., Klein, M. I., Falsetta, M. L., Lu, B., Delahunty, C. M., Yates, J. R., Heydorn, A., & Koo, H. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002623 · Cited by 514 · see citing works
Cooperation and conflict in microbial biofilms
Xavier, J. B., & Foster, K. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607651104 · Cited by 514 · see citing works
Kreth, J., Zhang, Y., & Herzberg, M. C. (2008) · Journal of Bacteriology · doi:10.1128/jb.00276-08 · Cited by 450 · see citing works
Tolédano, M. B., Kullik, I., Trinh, F., Baird, P. T., Schneider, T. D., & Storz, G. (1994) · Cell · doi:10.1016/s0092-8674(94)90702-1 · Cited by 389 · see citing works
Pericone, C. D., Overweg, K., Hermans, P. W. M., & Weiser, J. N. (2000) · Infection and Immunity · doi:10.1128/iai.68.7.3990-3997.2000 · Cited by 374 · see citing works
An in vivo polymicrobial biofilm wound infection model to study interspecies interactions
Dalton, T., Dowd, S. E., Wolcott, R. D., Sun, Y., Watters, C., Griswold, J. A., & Rumbaugh, K. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027317 · Cited by 372 · see citing works
Self-citationValm, A. M., Welch, J. L. M., Rieken, C. W., Hasegawa, Y., Sogin, M. L., Oldenbourg, R., Dewhirst, F. E., & Borisy, G. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101134108 · Cited by 340 · see citing works
Emergence of Spatial Structure in Cell Groups and the Evolution of Cooperation
Nadell, C. D., Foster, K. R., & Xavier, J. B. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000716 · Cited by 335 · see citing works
Korgaonkar, A., Trivedi, U., Rumbaugh, K. P., & Whiteley, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214550110 · Cited by 315 · see citing works
Self-citationKaplan, J. B., Velliyagounder, K., Ragunath, C., Rohde, H., Mack, D., Knobloch, J. K.-M., & Ramasubbu, N. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.24.8213-8220.2004 · Cited by 301 · see citing works
Metabolite Cross-Feeding Enhances Virulence in a Model Polymicrobial Infection
Ramsey, M. M., Rumbaugh, K. P., & Whiteley, M. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002012 · Cited by 238 · see citing works
Self-citationArmbruster, C. E., Hong, W., Pang, B., Weimer, K. E. D., Juneau, R. A., Turner, J. D., & Swords, W. E. (2010) · mBio · doi:10.1128/mbio.00102-10 · Cited by 220 · see citing works
Goodson, J. M. (2003) · Periodontology 2000 · doi:10.1034/j.1600-0757.2003.03104.x · Cited by 204 · see citing works
Strong inter-population cooperation leads to partner intermixing in microbial communities
Momeni, B., Brileya, K. A., Fields, M. W., & Shou, W. (2013) · eLife · doi:10.7554/elife.00230 · Cited by 199 · see citing works
Infection Due to Actinobacillus actinomycetemcomitans: 15 Cases and Review
Kaplan, A. H., Weber, D. J., Oddone, E. Z., & Perfect, J. R. (1989) · Clinical Infectious Diseases · doi:10.1093/clinids/11.1.46 · Cited by 197 · see citing works
Loesche, W. J., Gusberti, F. A., Mettraux, G., Higgins, T., & Syed, S. A. (1983) · Infection and Immunity · doi:10.1128/iai.42.2.659-667.1983 · Cited by 196 · see citing works
Molecular Pathogenicity of the Oral Opportunistic PathogenActinobacillus actinomycetemcomitans
Henderson, B. E., Nair, S. P., Ward, J. M., & Wilson, M. (2003) · Annual Review of Microbiology · doi:10.1146/annurev.micro.57.030502.090908 · Cited by 183 · see citing works
Liu, X., Ramsey, M. M., Chen, X., Koley, D., Whiteley, M., & Bard, A. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018391108 · Cited by 176 · see citing works
Self-citationRamsey, M. M., & Whiteley, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809533106 · Cited by 168 · see citing works
Self-citationSchreiner, H. C., Sinatra, K., Kaplan, J. B., Furgang, D., Kachlany, S. C., Planet, P. J., Perez, B. A., Figurski, D. H., & Fine, D. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1237223100 · Cited by 166 · see citing works
Kachlany, S. C., Planet, P. J., DeSalle, R., Fine, D. H., & Figurski, D. H. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02161-8 · Cited by 155 · see citing works
Aggregatibacter actinomycetemcomitans Leukotoxin
Kachlany, S. C. (2010) · Journal of Dental Research · doi:10.1177/0022034510363682 · Cited by 151 · see citing works
Kolenbrander, P. E., Andersen, R. N., & Moore, L. V. H. (1990) · Applied and Environmental Microbiology · doi:10.1128/aem.56.12.3890-3894.1990 · Cited by 136 · see citing works
Bacteriology of dental abscesses of endodontic origin
Williams, B. L., McCANN, G. F., & Schoenknecht, F. D. (1983) · Journal of Clinical Microbiology · doi:10.1128/jcm.18.4.770-774.1983 · Cited by 131 · see citing works
Jakubovics, N. S., Gill, S. R., Vickerman, M. M., & Kolenbrander, P. E. (2008) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2008.00585.x · Cited by 128 · see citing works
Korgaonkar, A. K., & Whiteley, M. (2010) · Journal of Bacteriology · doi:10.1128/jb.01175-10 · Cited by 121 · see citing works
Self-citationBrown, S. A., & Whiteley, M. (2007) · Journal of Bacteriology · doi:10.1128/jb.00554-07 · Cited by 115 · see citing works
Self-citationEffects Of H2 O2-Producing Lactobacilli On Neisseria gonorrhoeae Growth and Activity
Zheng, H.-Y., Alcorn, T. M., & Cohen, M. S. (1994) · The Journal of Infectious Diseases · doi:10.1093/infdis/170.5.1209 · Cited by 106 · see citing works
Yoneda, M., Hirofuji, T., Anan, H., Matsumoto, A., Hamachi, T., Nakayama, K., & Maeda, K. (2001) · Journal of Periodontal Research · doi:10.1034/j.1600-0765.2001.036004237.x · Cited by 105 · see citing works
Rahamat-Langendoen, J. C., van Vonderen, M. G. A., Engström, L. J., Manson, W. L., Winkelhoff, A. J. V., & Mooi-Kokenberg, E. A. N. M. (2011) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2011.01737.x · Cited by 87 · see citing works
Estrela, S., & Brown, S. P. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003398 · Cited by 84 · see citing works
Kesavalu, L. N., Holt, S. C., & Ebersole, J. L. (1998) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1998.tb00694.x · Cited by 80 · see citing works
Biofilm Dispersal of Neisseria subflava and Other Phylogenetically Diverse Oral Bacteria
Kaplan, J. B., & Fine, D. H. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.10.4943-4950.2002 · Cited by 79 · see citing works
Comparative virulence of periodontopathogens in a mouse abscess model
Ebersole, J. L., Kesavaln, L., Schneider, S., Machen, R. L., & Holt, S. (1995) · Oral Diseases · doi:10.1111/j.1601-0825.1995.tb00174.x · Cited by 78 · see citing works
Influence of Environmental Conditions on Hydrogen Peroxide Formation by Streptococcus gordonii
Barnard, J. P., & Stinson, M. W. (1999) · Infection and Immunity · doi:10.1128/iai.67.12.6558-6564.1999 · Cited by 67 · see citing works
Ymele‐Leki, P., & Ross, J. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01319-06 · Cited by 61 · see citing works
Transport phenomena of microbial flora in the small intestine with peristalsis
Ishikawa, T., Sato, T., Mohit, G., Imai, Y., & Yamaguchi, T. (2011) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2011.03.026 · Cited by 59 · see citing works
Probing Bacterial Metabolism during Infection Using High-Resolution Transcriptomics
Jorth, P. A., Trivedi, U., Rumbaugh, K. P., & Whiteley, M. (2013) · Journal of Bacteriology · doi:10.1128/jb.00875-13 · Cited by 52 · see citing works
Self-citationDaims, H., & Wagner, M. (2011) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-386489-5.00008-7 · Cited by 51 · see citing works
Schillinger, C., Petrich, A., Lux, R., Riep, B., Kikhney, J., Friedmann, A., Wolinsky, L. E., Göbel, U. B., Daims, H., & Moter, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037583 · Cited by 48 · see citing works
Hillman, J. D., & Shivers, M. (1988) · Archives of Oral Biology · doi:10.1016/0003-9969(88)90196-3 · Cited by 48 · see citing works
Madeira, M. F. M., Queiroz‐Junior, C. M., Cisalpino, D., Werneck, S. M. C., Kikuchi, H., Fujise, O., Ryffel, B., Silva, T. A., Teixeira, M. M., & Souza, D. G. (2013) · Molecular Oral Microbiology · doi:10.1111/omi.12034 · Cited by 37 · see citing works
Teng, Y.-T. A., & Zhang, X. (2005) · Microbial Pathogenesis · doi:10.1016/j.micpath.2004.12.004 · Cited by 22 · see citing works
Schreiner, H. C., Li, Y., Cline, J., Tsiagbe, V. K., & Fine, D. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069382 · Cited by 18 · see citing works
Li, L., Ding, C., Duan, J.-L., Yang, M., Sun, Y., Wang, X., & Xu, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065729 · Cited by 10 · see citing works
Fetiye, K., Karadenizli, A., Okay, E., Oz, S., Budak, F., Gündeş, S., & Vahaboğlu, H. (2004) · Annals of Clinical Microbiology and Antimicrobials · doi:10.1186/1476-0711-3-2 · Cited by 10 · see citing works
[Streptococcus gordonii extensive multiple subcutanoeus abscesses].
Esposito, S., Avallone, L., Massari, A., Pardo, D. L., Pezzuti, G., Smaldone, P., Anzalone, S., & Ardimento, P. (2011) · PubMed · Cited by 4 · see citing works
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- [17]17. Madeira MF, et al. (2013) MyD88 is essential for alveolar bone loss induced by Ag- gregatibacter actinomycetemcomitans lipopolysaccharide in mice. Mol Oral Microbiol 28(6):415-424.
Cited by
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The Oral Microbiota: Dynamic Communities and Host Interactions
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0089-x · Cited by 2,217 · see citing works
Progress in and promise of bacterial quorum sensing research
Whiteley, M., Diggle, S. P., & Greenberg, E. P. (2017) · Nature · doi:10.1038/nature24624 · Cited by 1,281 · see citing works
Self-citationPolymicrobial synergy and dysbiosis in inflammatory disease
Lamont, R. J., & Hajishengallis, G. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.11.004 · Cited by 585 · see citing works
Dental biofilm: ecological interactions in health and disease
Marsh, P., & Zaura, E. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12679 · Cited by 569 · see citing works
The dental plaque biofilm matrix
Jakubovics, N. S., Goodman, S. D., Mashburn‐Warren, L., Stafford, G. P., & Cieplik, F. (2021) · Periodontology 2000 · doi:10.1111/prd.12361 · Cited by 488 · see citing works
The biogeography of polymicrobial infection
Stacy, A., McNally, L., Darch, S. E., Brown, S. P., & Whiteley, M. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2015.8 · Cited by 288 · see citing works
Self-citationShort-range interactions govern the dynamics and functions of microbial communities
Co, A. D., van Vliet, S., Kiviet, D. J., Schlegel, S., & Ackermann, M. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-019-1080-2 · Cited by 289 · see citing works
Escaping the biofilm in more than one way: desorption, detachment or dispersion
Petrova, O. E., & Sauer, K. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2016.01.004 · Cited by 288 · see citing works
Role of microbial communities in the pathogenesis of periodontal diseases and caries
Mira, Á., Simón‐Soro, Á., & Curtis, M. A. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12671 · Cited by 283 · see citing works
Hajishengallis, G., & Lamont, R. J. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.02.010 · Cited by 275 · see citing works
“Such ‘fight and flight’ interactions can lead to defined spatial arrangements of the various species within communities, thereby optimizing the function of the community as a whole [28].”
BackgroundGuilhen, C., Forestier, C., & Balestrino, D. (2017) · Molecular Microbiology · doi:10.1111/mmi.13698 · Cited by 226 · see citing works
Oral polymicrobial communities: Assembly, function, and impact on diseases
Hajishengallis, G., Lamont, R. J., & Koo, H. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2023.02.009 · Cited by 221 · see citing works
The importance of understanding the infectious microenvironment
Bjarnsholt, T., Whiteley, M., Rumbaugh, K. P., Stewart, P. S., Jensen, P. Ø., & Frimodt-Møller, N. (2021) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(21)00122-5 · Cited by 211 · see citing works
Self-citationVaumourin, E., Vourc’h, G., Gasqui, P., & Vayssier‐Taussat, M. (2015) · Parasites & Vectors · doi:10.1186/s13071-015-1167-9 · Cited by 189 · see citing works
Connell, J. L., Kim, J., Shear, J. B., Bard, A. J., & Whiteley, M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421211111 · Cited by 181 · see citing works
Self-citationPathogens protection against the action of disinfectants in multispecies biofilms
Sanchez-Vizuete, P., Orgaz, B., Aymerich, S., Coq, D. L., & Briandet, R. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00705 · Cited by 156 · see citing works
Smith, K., Collier, A., Townsend, E. R., O’Donnell, L. E., Bal, A. M., Butcher, J. P., Mackay, W. G., Ramage, G., & Williams, C. (2016) · BMC Microbiology · doi:10.1186/s12866-016-0665-z · Cited by 153 · see citing works
Spatial determinants of quorum signaling in a Pseudomonas aeruginosa infection model
Darch, S. E., Simoska, O., Fitzpatrick, M. D., Barraza, J. P., Stevenson, K. J., Bonnecaze, R. T., Shear, J. B., & Whiteley, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719317115 · Cited by 147 · see citing works
Self-citationFine, D. H., Patil, A. G., & Velusamy, S. K. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00728 · Cited by 136 · see citing works
The diabetic foot microbiota: A review
Jneid, J., Lavigne, J., Scola, B. L., & Cassir, N. (2017) · Human Microbiome Journal · doi:10.1016/j.humic.2017.09.002 · Cited by 130 · see citing works
Formation, Development, and Cross-Species Interactions in Biofilms
Luo, A., Wang, F., DeGang, S., Liu, X., & Xin, B. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.757327 · Cited by 118 · see citing works
Redanz, S., Cheng, X., Giacaman, R. A., Pfeifer, C. S., Merritt, J. L., & Kreth, J. (2018) · Molecular Oral Microbiology · doi:10.1111/omi.12231 · Cited by 111 · see citing works
A multidimensional perspective on microbial interactions
Pacheco, A. R., & Segrè, D. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fnz125 · Cited by 105 · see citing works
Denture Stomatitis: Causes, Cures and Prevention
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Jakubovics, N. S. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.09.022 · Cited by 107 · see citing works
Antimicrobial effects of commensal oral species are regulated by environmental factors
Herrero, E. R., Slomka, V., Bernaerts, K., Boon, N., Hernandez‐Sanabria, E., Passoni, B. B., Quirynen, M., & Teughels, W. (2016) · Journal of Dentistry · doi:10.1016/j.jdent.2016.02.007 · Cited by 105 · see citing works
Community interactions and spatial structure shape selection on antibiotic resistant lineages
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Lukumbuzya, M., Schmid, M. C., Pjevac, P., & Daims, H. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01383 · Cited by 98 · see citing works
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Røder, H. L., Olsen, N. M. C., Whiteley, M., & Burmølle, M. (2019) · Environmental Microbiology · doi:10.1111/1462-2920.14834 · Cited by 92 · see citing works
Self-citationAyala, F. R., Bartolini, M., & Grau, R. R. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01761 · Cited by 92 · see citing works
Liu, S., Rodriguez, J. S., Munteanu, V., Ronkowski, C., Sharma, N. K., Alser, M., Andreace, F., Blekhman, R., Błaszczyk, D., Chikhi, R., et al. (2025) · Nature Reviews Methods Primers · doi:10.1038/s43586-024-00376-6 · Cited by 92 · see citing works
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Phage Inhibit Pathogen Dissemination by Targeting Bacterial Migrants in a Chronic Infection Model
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Decoding molecular interactions in microbial communities
Abreu, N. A., & Taga, M. E. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw019 · Cited by 76 · see citing works
Liu, C., Ponsero, A. J., Armstrong, D. G., Lipsky, B. A., & Hurwitz, B. L. (2020) · BMC Medicine · doi:10.1186/s12916-020-01820-6 · Cited by 75 · see citing works
The social life of microbes in chronic infection
Ibberson, C. B., & Whiteley, M. (2020) · Current Opinion in Microbiology · doi:10.1016/j.mib.2020.02.003 · Cited by 73 · see citing works
Self-citationThe spatial and metabolic basis of colony size variation
Chacón, J. M., Möbius, W., & Harcombe, W. R. (2018) · The ISME Journal · doi:10.1038/s41396-017-0038-0 · Cited by 71 · see citing works
A crucial role for spatial distribution in bacterial quorum sensing
Gao, M., Zheng, H., Ren, Y., Lou, R., Wu, F., Yu, W., Liu, X., & Ma, X. (2016) · Scientific Reports · doi:10.1038/srep34695 · Cited by 67 · see citing works
Application of a quantitative framework to improve the accuracy of a bacterial infection model
Lewin, G. R., Kapur, A., Cornforth, D. M., Duncan, R. P., Diggle, F. L., Moustafa, D. A., Harrison, S., Skaar, E. P., Chazin, W., Goldberg, J. B., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2221542120 · Cited by 61 · see citing works
Self-citationDual lifestyle of Porphyromonas gingivalis in biofilm and gingival cells
Sakanaka, A., Takeuchi, H., Kuboniwa, M., & Amano, A. (2015) · Microbial Pathogenesis · doi:10.1016/j.micpath.2015.10.003 · Cited by 66 · see citing works
Ishikawa, K. H., Bueno, M. R., Kawamoto, D., Simionato, M. R. L., & Mayer, M. P. A. (2021) · Molecular Oral Microbiology · doi:10.1111/omi.12330 · Cited by 64 · see citing works
The biogeography of infection revisited
Azimi, S., Lewin, G. R., & Whiteley, M. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00683-3 · Cited by 60 · see citing works
Self-citationJakubovics, N. S. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mbp-0013-2014 · Cited by 62 · see citing works
Efficacy and safety of biofilm dispersal by glycoside hydrolases in wounds
Redman, W. K., Welch, G. S., Williams, A. C., Damron, A. J., Northcut, W. O., & Rumbaugh, K. P. (2021) · Biofilm · doi:10.1016/j.bioflm.2021.100061 · Cited by 59 · see citing works
Self-citationTowards improved biofilm models
Rumbaugh, K. P., & Whiteley, M. (2024) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01086-2 · Cited by 63 · see citing works
Self-citationBacterial interactions in pathogenic subgingival plaque
Ng, H. M., Kin, L. X., Dashper, S. G., Slakeski, N., Butler, C. A., & Reynolds, E. C. (2015) · Microbial Pathogenesis · doi:10.1016/j.micpath.2015.10.022 · Cited by 61 · see citing works
Alterations of microbiota structure in the larynx relevant to laryngeal carcinoma
Gong, H., Shi, Y., Xiao, X., Cao, P., Wu, C., Tao, L., Hou, D., Wang, Y., & Zhou, L. F. (2017) · Scientific Reports · doi:10.1038/s41598-017-05576-7 · Cited by 59 · see citing works
Vuong, H. Q., & McFrederick, Q. S. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz136 · Cited by 58 · see citing works
Metabolic Signaling and Spatial Interactions in the Oral Polymicrobial Community
Miller, D. P., Fitzsimonds, Z. R., & Lamont, R. J. (2019) · Journal of Dental Research · doi:10.1177/0022034519866440 · Cited by 56 · see citing works
Zhu, B., Macleod, L. C., Newsome, E., Liu, J., & Xu, P. (2019) · Scientific Reports · doi:10.1038/s41598-019-41467-9 · Cited by 55 · see citing works
Verza, B. S., van den Beucken, J. J. J. P., Brandt, J. V., Jafelicci, M., Barão, V. A. R., Piazza, R. D., Tagit, O., Spolidório, D. M. P., Vergani, C. E., & de Ávila, É. D. (2021) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2020.117604 · Cited by 55 · see citing works
Barraza, J. P., & Whiteley, M. (2021) · mBio · doi:10.1128/mbio.00047-21 · Cited by 47 · see citing works
Self-citationVirulence as a Side Effect of Interspecies Interaction in Vibrio Coral Pathogens
Rubio‐Portillo, E., Martín-Cuadrado, A.-B., Caraballo‐Rodríguez, A. M., Rohwer, F. L., Dorrestein, P. C., & Antón, J. (2020) · mBio · doi:10.1128/mbio.00201-20 · Cited by 48 · see citing works
Illuminating the oral microbiome and its host interactions: animal models of disease
Hajishengallis, G. (2023) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuad018 · Cited by 46 · see citing works
Aggregatibacter actinomycetemcomitans Dispersin B: The Quintessential Antibiofilm Enzyme
Kaplan, J. B., Sukhishvili, S. A., Sailer, M., Kridin, K., & Ramasubbu, N. (2024) · Pathogens · doi:10.3390/pathogens13080668 · Cited by 46 · see citing works
Duan, D., Scoffield, J. A., Zhou, X., & Wu, H. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13425 · Cited by 46 · see citing works
Polymicrobial Interactions of Oral Microbiota: a Historical Review and Current Perspective
Zhang, M., Whiteley, M., & Lewin, G. R. (2022) · mBio · doi:10.1128/mbio.00235-22 · Cited by 46 · see citing works
Self-citationYekani, M., Dastgir, M., Fattahi, S., Shahi, S., Dizaj, S. M., & Memar, M. Y. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1533658 · Cited by 50 · see citing works
Lewin, G. R., Stacy, A., Michie, K. L., Lamont, R. J., & Whiteley, M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907619116 · Cited by 41 · see citing works
Self-citationPark, B., Koh, H., Patatanian, M., Reyes-Caballero, H., Zhao, N., Meinert, J. L., Holbrook, J. T., Leinbach, L. I., & Biswal, S. S. (2023) · BMC Microbiology · doi:10.1186/s12866-023-02779-z · Cited by 45 · see citing works
Szafrański, S. P., Deng, Z.-L., Tomasch, J., Jarek, M., Bhuju, S., Rohde, M., Sztajer, H., & Wagner‐Döbler, I. (2017) · BMC Genomics · doi:10.1186/s12864-017-3618-5 · Cited by 44 · see citing works
Candida albicans: Molecular interactions with Pseudomonas aeruginosa and Staphylococcus aureus
Lindsay, A. K., & Hogan, D. A. (2014) · Fungal Biology Reviews · doi:10.1016/j.fbr.2014.10.002 · Cited by 42 · see citing works
The Inhibitory Effects of Ficin on Streptococcus mutans Biofilm Formation
Sun, Y., Jiang, W., Zhang, M., Zhang, L., Shen, Y., Huang, S., Li, M., Qiu, W., Pan, Y., Zhou, L., et al. (2021) · BioMed Research International · doi:10.1155/2021/6692328 · Cited by 41 · see citing works
Zhang, Y., Li, Y., Yang, Y., Wang, Y., Cao, X., Jin, Y., Xu, Y., Li, S. C., & Zhou, Q. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.785191 · Cited by 42 · see citing works
Emotional affordances for human–robot interaction
Vallverdú, J., & Trovato, G. (2016) · Adaptive Behavior · doi:10.1177/1059712316668238 · Cited by 40 · see citing works
Wei, H., Li, X., Tang, L., Yao, H., Ren, Z., Wang, C., Mu, C., Shi, C., & Wang, H. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.126891 · Cited by 40 · see citing works
Microbial Community Composition Impacts Pathogen Iron Availability during Polymicrobial Infection
Stacy, A., Abraham, N., Jorth, P. A., & Whiteley, M. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1006084 · Cited by 39 · see citing works
Self-citationStreptococcus sanguinis induces neutrophil cell death by production of hydrogen peroxide
Sumioka, R., Nakata, M., Okahashi, N., Li, Y., Wada, S., Yamaguchi, M., Sumitomo, T., Hayashi, M., & Kawabata, S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172223 · Cited by 39 · see citing works
Social networking at the microbiome-host interface
Lamont, R. J., Hajishengallis, G., & Koo, H. (2023) · Infection and Immunity · doi:10.1128/iai.00124-23 · Cited by 38 · see citing works
Insights into Dynamic Polymicrobial Synergy Revealed by Time-Coursed RNA-Seq
Hendrickson, E. L., Beck, D. A. C., Miller, D. P., Wang, Q., Whiteley, M., Lamont, R. J., & Hackett, M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00261 · Cited by 38 · see citing works
Self-citationRegulation of Biofilm Aging and Dispersal in Bacillus subtilis by the Alternative Sigma Factor SigB
Bartolini, M., Cogliati, S., Vileta, D., Bauman, C., Rateni, L., Leñini, C., Argañaraz, F., Francisco, M., Villalba, J. M., Steil, L., et al. (2018) · Journal of Bacteriology · doi:10.1128/jb.00473-18 · Cited by 36 · see citing works
Wang, X., Jiang, C., Wang, D., Yang, Y., Fan, L., Xu, S., & Zhuang, X. (2023) · Water Research · doi:10.1016/j.watres.2023.119993 · Cited by 36 · see citing works
Transcriptional responses of Streptococcus gordonii and Fusobacterium nucleatum to coaggregation
Mutha, N. V. R., Mohammed, W. K., Krasnogor, N., Tan, G. Y. A., Choo, S. W., & Jakubovics, N. S. (2018) · Molecular Oral Microbiology · doi:10.1111/omi.12248 · Cited by 34 · see citing works
Aggregatibacter actinomycetemcomitans and Filifactor alocis: Two exotoxin-producing oral pathogens
Ozuna, H., Snider, I., Belibasakis, G. N., Oscarsson, J., Johansson, A., & Uriarte, S. M. (2022) · Frontiers in Oral Health · doi:10.3389/froh.2022.981343 · Cited by 33 · see citing works
Price, K. E., Naimie, A. A., Griffin, E. F., Bay, C., & O’Toole, G. A. (2015) · Journal of Bacteriology · doi:10.1128/jb.00705-15 · Cited by 32 · see citing works
Back, C. R., Douglas, S., Emerson, J. E., Nobbs, A. H., & Jenkinson, H. F. (2015) · Molecular Oral Microbiology · doi:10.1111/omi.12106 · Cited by 32 · see citing works
The demographic determinants of human microbiome health
Estrela, S., Whiteley, M., & Brown, S. P. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2014.11.005 · Cited by 31 · see citing works
Self-citationScoffield, J. A., & Wu, H. (2015) · Microbiology · doi:10.1099/mic.0.000226 · Cited by 30 · see citing works
The Oral Microbiome of Peri-Implant Health and Disease: A Narrative Review
de Campos, N., Buischi, Y. D. P., Mohamadzadeh, M., & Loomer, P. M. (2024) · Dentistry Journal · doi:10.3390/dj12100299 · Cited by 33 · see citing works
Keshvardoust, P., Huron, V. A. A., Clemson, M., Constancias, F., Barraud, N., & Rice, S. A. (2019) · npj Biofilms and Microbiomes · doi:10.1038/s41522-019-0095-4 · Cited by 29 · see citing works
From Nursery to Nursing Home: Emerging Concepts in Clostridioides difficile Pathogenesis
Smith, A. B., Ocaña, J. S., & Zackular, J. P. (2020) · Infection and Immunity · doi:10.1128/iai.00934-19 · Cited by 28 · see citing works
Shakya, S., Danshiitsoodol, N., Noda, M., Inoue, Y., & Sugiyama, M. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.991144 · Cited by 28 · see citing works
Pajon, C., Fortoul, M. C., Diaz-Tang, G., Meneses, E. M., Kalifa, A. R., Sevy, E., Mariah, T., Toscan, B., Marcelin, M., Hernandez, D. M., et al. (2023) · eLife · doi:10.7554/elife.83664 · Cited by 27 · see citing works
Melnik, A. V., Vázquez‐Baeza, Y., Aksenov, A. A., Hyde, E. R., McAvoy, A. C., Wang, M., Silva, R., Protsyuk, I., Wu, J. V., Bouslimani, A., et al. (2019) · mSystems · doi:10.1128/msystems.00375-19 · Cited by 27 · see citing works
P. aeruginosa interactions with other microbes in biofilms during co-infection
Oliveira, M., Cunha, E. S., Tavares, L. M., & Serrano, I. D. (2023) · AIMS Microbiology · doi:10.3934/microbiol.2023032 · Cited by 27 · see citing works
The polymicrobial pathogenicity of Porphyromonas gingivalis
Lamont, R. J., & Kuboniwa, M. (2024) · Frontiers in Oral Health · doi:10.3389/froh.2024.1404917 · Cited by 27 · see citing works
Cheng, X., Redanz, S., Treerat, P., Qin, H., Choi, D., Zhou, X., Xu, X., Merritt, J. L., & Kreth, J. (2020) · Journal of Dental Research · doi:10.1177/0022034520912181 · Cited by 26 · see citing works
Biofilms 2015: Multidisciplinary Approaches Shed Light into Microbial Life on Surfaces
Visick, K. L., Schembri, M. A., Yildiz, F. H., & Ghigo, J. (2016) · Journal of Bacteriology · doi:10.1128/jb.00156-16 · Cited by 26 · see citing works
Sharma, K., Mudgil, P., Whitehall, J. S., & Gosbell, I. B. (2017) · Annals of Clinical Microbiology and Antimicrobials · doi:10.1186/s12941-017-0186-0 · Cited by 25 · see citing works
Darch, S. E., & Koley, D. (2018) · Proceedings of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rspa.2018.0405 · Cited by 25 · see citing works
From molecules to multispecies ecosystems: the roles of structure in bacterial biofilms
Gordon, V. D., Bakhtiari, L. A., & Kovach, K. N. (2019) · Physical Biology · doi:10.1088/1478-3975/ab1384 · Cited by 24 · see citing works
Regulation of olfactomedin 4 by Porphyromonas gingivalis in a community context
Fitzsimonds, Z. R., Liu, C., Stocke, K. S., Yakoumatos, L., Shumway, B. S., Miller, D. P., Artyomov, M. N., Bagaitkar, J., & Lamont, R. J. (2021) · The ISME Journal · doi:10.1038/s41396-021-00956-4 · Cited by 23 · see citing works
Trivedi, U., Madsen, J. S., Rumbaugh, K. P., Wolcott, R. D., Burmølle, M., & Sørensen, S. J. (2016) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2016.1252312 · Cited by 23 · see citing works
Self-citationZou, D., Deng, K., Zeng, Z., Gong, W., Guo, B., Liu, Y., Xie, Y., Li, Y., & Xu, X. (2025) · Journal of the American Chemical Society · doi:10.1021/jacs.5c10219 · Cited by 22 · see citing works
- Authors
- Stacy, A., Everett, J., Jorth, P., Trivedi, U., Rumbaugh, K. P., & Whiteley, M.
- Affiliations
- The University of Texas at Austin (US)
- Texas Tech University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-05-13
- Volume
- 111
- Issue
- 21
- Pages
- 7819-7824
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4040543
- OpenAlex
- W2088151791
- Cited by
- 192
- References
- 58
- Citations by year
- 2026: 4 · 2025: 12 · 2024: 22 · 2023: 16 · 2022: 14 · 2021: 12 · 2020: 19 · 2019: 20 · 2018: 12 · 2017: 21 · 2016: 18 · 2015: 15 · 2014: 7
- FWCI
- 8.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Dental and Craniofacial Research (R01DE020100)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Aggregatibacter actinomycetemcomitans, Streptococcus gordonii, co-infection, cross-feeding, hydrogen peroxide, dispersin B, biofilm dispersal, fight-or-flight response, oral infection, virulence
- MeSH terms
- Animals, Bacterial Proteins, Catalase, Glycoside Hydrolases, Hydrogen Peroxide, Virulence, Aggregatibacter actinomycetemcomitans, Biofilms, Lactic Acid, Microarray Analysis, Mice, Streptococcus gordonii, Coinfection
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