Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection
Open accessAbstract
Most infections result from colonization by more than one microbe. Within such polymicrobial infections, microbes often display synergistic interactions that result in increased disease severity. Although many clinical studies have documented the occurrence of synergy in polymicrobial infections, little is known about the underlying molecular mechanisms. A prominent pathogen in many polymicrobial infections is Pseudomonas aeruginosa, a Gram-negative bacterium that displays enhanced virulence during coculture with Gram-positive bacteria. In this study we discovered that during coinfection, P. aeruginosa uses peptidoglycan shed by Gram-positive bacteria as a cue to stimulate production of multiple extracellular factors that possess lytic activity against prokaryotic and eukaryotic cells. Consequently, P. aeruginosa displays enhanced virulence in a Drosophila model of infection when cocultured with Gram-positive bacteria. Inactivation of a gene (PA0601) required for peptidoglycan sensing mitigated this phenotype. Using Drosophila and murine models of infection, we also show that peptidoglycan sensing results in P. aeruginosa-mediated reduction in the Gram-positive flora in the infection site. Our data suggest that P. aeruginosa has evolved a mechanism to survey the microbial community and respond to Gram-positive produced peptidoglycan through production of antimicrobials and toxins that not only modify the composition of the community but also enhance host killing. Additionally, our results suggest that therapeutic strategies targeting Gram-positive bacteria might be a viable approach for reducing the severity of P. aeruginosa polymicrobial infections.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Peptidoglycan fragments may play roles in more mature biofilms as environmental cues, since they regulate processes such as germination of spores in Bacillus, production of antimicrobial compounds by P. aeruginosa, and yeast-hyphal transition in C. albicans.
“peptidoglycan fragments may play roles in more mature biofilms as environmental cues, since it has been demonstrated that they regulate processes such as the germination of spores in Bacillus, the production of antimicrobial compounds by P. aeruginosa, and the yeast-hyphal transition in C. albicans.173–175”
From The dental plaque biofilm matrix (2021) · cites this paper as [175]
Cites
Nod2 Is a General Sensor of Peptidoglycan through Muramyl Dipeptide (MDP) Detection
Girardin, S. E., Boneca, I. G., Viala, J., Chamaillard, M., Labigne-Roussel, A., Thomas, G. D., Philpott, D. J., & Sansonetti, P. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c200651200 · Cited by 2,397 · see citing works
Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases
Merzendorfer, H., & Zimoch, L. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00709 · Cited by 1,251 · see citing works
Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa
Pesci, E. C., Milbank, J. B. J., Pearson, J. P., McKnight, S. L., Kende, A. S., Greenberg, E. P., & Iglewski, B. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11229 · Cited by 1,115 · see citing works
An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants
Liberati, N. T., Urbach, J. M., Miyata, S., Lee, D. G., Drenkard, E., Wu, G., Villanueva, J. M., Wei, T., & Ausubel, F. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511100103 · Cited by 971 · see citing works
Essar, D. W., Eberly, L., Hadero, A., & Crawford, I. P. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.2.884-900.1990 · Cited by 929 · 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
Mahajan‐Miklos, S., Tan, M., Rahme, L. G., & Ausubel, F. M. (1999) · Cell · doi:10.1016/s0092-8674(00)80958-7 · Cited by 821 · 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
Diggle, S. P., Winzer, K., Chhabra, S. R., Worrall, K. E., Cámara, M., & Williams, P. M. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03672.x · Cited by 623 · see citing works
Multiple bacterial species reside in chronic wounds: a longitudinal study
Gjødsbøl, K., Christensen, J. J., Karlsmark, T., Jørgensen, B., Klein, B. M., & Krogfelt, K. A. (2006) · International Wound Journal · doi:10.1111/j.1742-481x.2006.00159.x · Cited by 623 · see citing works
Dowd, S. E., Wolcott, R. D., Sun, Y., McKeehan, T., Smith, E., & Rhoads, D. D. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003326 · Cited by 562 · see citing works
Distribution, Organization, and Ecology of Bacteria in Chronic Wounds
Kirketerp‐Møller, K., Jensen, P. Ø., Fazli, M., Madsen, K. G., Pedersen, J., Moser, C. E., Tolker‐Nielsen, T., Høiby, N., Givskov, M., & Bjarnsholt, T. (2008) · Journal of Clinical Microbiology · doi:10.1128/jcm.00501-08 · Cited by 547 · see citing works
Duan, K., Dammel, C., Stein, J., Rabin, H. R., & Surette, M. G. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03803.x · Cited by 510 · see citing works
Diggle, S. P., Matthijs, S., Wright, V. J., Fletcher, M. P., Chhabra, S. R., Lamont, I. L., Kong, X., Hider, R. C., Cornélis, P., Cámara, M., et al. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2006.11.014 · Cited by 500 · see citing works
Nonrandom Distribution of Pseudomonas aeruginosa and Staphylococcus aureus in Chronic Wounds
Fazli, M., Bjarnsholt, T., Kirketerp‐Møller, K., Jørgensen, B., Andersen, A. S., Krogfelt, K. A., Givskov, M., & Tolker‐Nielsen, T. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.01395-09 · Cited by 496 · see citing works
Shah, I. M., Laaberki, M.-H., Popham, D. L., & Dworkin, J. (2008) · Cell · doi:10.1016/j.cell.2008.08.039 · Cited by 489 · see citing works
QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa
Chugani, S. A., Whiteley, M., Lee, K. M., D’Argenio, D. A., Manoil, C., & Greenberg, E. P. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051624298 · Cited by 446 · see citing works
Self-citationPlants and animals share functionally common bacterial virulence factors
Rahme, L. G., Ausubel, F. M., Cao, H., Drenkard, E., Goumnerov, B. C., Lau, G. W., Mahajan‐Miklos, S., Plotnikova, J. M., Tan, M., Tsongalis, J., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.16.8815 · Cited by 416 · 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-citationImmunochemical Properties of the Staphylococcal Poly- N -Acetylglucosamine Surface Polysaccharide
Maira‐Litrán, T., Kropec, A., Abeygunawardana, C., Joyce, J. G., Mark, G. E., Goldmann, D. A., & Pier, G. B. (2002) · Infection and Immunity · doi:10.1128/iai.70.8.4433-4440.2002 · Cited by 324 · see citing works
Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease.
Kessler, E., Safrin, M., Olson, J. C., & Ohman, D. E. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53203-8 · Cited by 324 · see citing works
Cox, C. R., & Gilmore, M. S. (2007) · Infection and Immunity · doi:10.1128/iai.01496-06 · Cited by 315 · see citing works
Mashburn, L. M., Jett, A. M., Akins, D. R., & Whiteley, M. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.2.554-566.2005 · Cited by 312 · see citing works
Self-citationQuorum Sensing and the Social Evolution of Bacterial Virulence
Rumbaugh, K. P., Diggle, S. P., Watters, C., Ross‐Gillespie, A., Griffin, A. S., & West, S. A. (2009) · Current Biology · doi:10.1016/j.cub.2009.01.050 · Cited by 302 · see citing works
Self-citationXu, X.-L., Lee, R. T. H., Fang, H.-M., Wang, Y.-M., Li, R., Zou, H., Zhu, Y., & Wang, Y. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.05.014 · Cited by 289 · see citing works
BJORNSON, H. S., COLLEY, R., Bower, R. H., Duty, V. P., Schwartz-Fulton, J., & Fischer, J. E. (1982) · PubMed · Cited by 272 · see citing works
Sibley, C. D., Duan, K., Fischer, C. D., Parkins, M. D., Storey, D. G., Rabin, H. R., & Surette, M. G. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000184 · Cited by 261 · 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
ISOLATION OF OLIGOSACCHARIDES ENZYMATICALLY PRODUCED FROM HYALURONIC ACID
Weissmann, B., Meyer, K., Sampson, P. M., & Linker, A. (1954) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)65660-1 · Cited by 200 · see citing works
Recent insights into the biological roles of mucin-type O-glycosylation
Tian, E., & Hagen, K. G. T. (2008) · Glycoconjugate Journal · doi:10.1007/s10719-008-9162-4 · Cited by 191 · see citing works
2-Heptyl-4-hydroxyquinoline N -oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa
Machan, Z. A., Taylor, G. W., Pitt, T. L., COLE, P. J., & Wilson, R. (1992) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/30.5.615 · Cited by 190 · see citing works
Elucidating the molecular mechanisms of bacterial virulence using non‐mammalian hosts
Mahajan‐Miklos, S., Rahme, L. G., & Ausubel, F. M. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.02056.x · Cited by 181 · see citing works
Ramsey, M. M., & Whiteley, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809533106 · Cited by 168 · see citing works
Self-citationDeveloping animal models for polymicrobial diseases
Bakaletz, L. O. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro928 · Cited by 158 · see citing works
Davies, C. E., Hill, K. E., Wilson, M. J., Stephens, P., Hill, C., Harding, K. G., & Thomas, D. W. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.8.3549-3557.2004 · Cited by 152 · see citing works
THE EFFECT OF BACTERIAL COLONIZATION ON VENOUS ULCER HEALING
Halbert, A., Stacey, M. C., Rohr, J. B., & Jopp‐McKay, A. G. (1992) · Australasian Journal of Dermatology · doi:10.1111/j.1440-0960.1992.tb00083.x · Cited by 131 · 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-citationMulcahy, H., Sibley, C. D., Surette, M. G., & Lewenza, S. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002299 · Cited by 114 · see citing works
A complex network regulates expression of eps and other virulence genes of Pseudomonas solanacearum
Huang, J., Carney, B., Denny, T. P., Weissinger, A. K., & Schell, M. A. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.5.1259-1267.1995 · Cited by 110 · see citing works
Wiener, E. S. (1983) · Journal of Pediatric Surgery · doi:10.1016/s0022-3468(83)80214-0 · Cited by 109 · see citing works
Weimer, K. E. D., Armbruster, C. E., Juneau, R. A., Hong, W., Pang, B., & Swords, W. E. (2010) · The Journal of Infectious Diseases · doi:10.1086/656046 · Cited by 102 · see citing works
Effect of Pyocyanin on a Crude-Oil-Degrading Microbial Community
Norman, R. S., Moeller, P. D. R., McDonald, T. J., & Morris, P. J. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.7.4004-4011.2004 · Cited by 93 · see citing works
Theopold, U., Samakovlis, C., Erdjument‐Bromage, H., Dillon, N., Axelsson, B., Schmidt, O., Tempst, P., & Hultmark, D. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.22.12708 · Cited by 90 · see citing works
Pseudomonas aeruginosa virulence genes identified in a Dictyostelium host model
Alibaud, L., Köhler, T., Coudray, A., Prigent‐Combaret, C., Bergeret, E., Perrin, J., Benghezal, M., Reimmann, C., Gauthier, Y., van Delden, C., et al. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.01080.x · Cited by 88 · 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
Weimer, K. E. D., Juneau, R. A., Murrah, K. A., Pang, B., Armbruster, C. E., Richardson, S. H., & Swords, W. E. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiq087 · Cited by 73 · see citing works
Synergy in Polymicrobial Infections in a Mouse Model of Type 2 Diabetes
Mastropaolo, M. D., Evans, N. P., Byrnes, M. K., Stevens, A. M., Robertson, J. L., & Melville, S. B. (2005) · Infection and Immunity · doi:10.1128/iai.73.9.6055-6063.2005 · Cited by 62 · see citing works
Nagashima, H., Takao, A., & Maeda, N. (1999) · Microbiology and Immunology · doi:10.1111/j.1348-0421.1999.tb02395.x · Cited by 60 · see citing works
Insight into the composition of the intercellular matrix of Streptococcus pneumoniae biofilms
Domenech, M., Garcı́a, E., Prieto, A., & Moscoso, M. (2012) · Environmental Microbiology · doi:10.1111/j.1462-2920.2012.02853.x · Cited by 58 · see citing works
Pseudomonas aeruginosa LasA Protease in Treatment of Experimental Staphylococcal Keratitis
Barequet, I. S., Simon, G. B., Safrin, M., Ohman, D. E., & Kessler, E. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.5.1681-1687.2004 · Cited by 51 · see citing works
Identification of mutants with altered phenazine production in Pseudomonas aeruginosa
Liang, H., Duan, J., Sibley, C. D., Surette, M. G., & Duan, K. (2010) · Journal of Medical Microbiology · doi:10.1099/jmm.0.022350-0 · Cited by 46 · see citing works
Wound-healing technologies: low-level laser and vacuum-assisted closure.
Samson, D. J., Lefevre, F., & Aronson, N. (2004) · PubMed Central · Cited by 40 · see citing works
The oligomeric structure of rat and human gastric mucins
Dekker, J. P., Aelmans, P. H., & Strous, G. J. (1991) · Biochemical Journal · doi:10.1042/bj2770423 · Cited by 38 · see citing works
Zero order kinetics of cell wall turnover inStaphylococcus aureus
Bl�mel, P., Uecker, W., & Giesbrecht, P. (1979) · Archives of Microbiology · doi:10.1007/bf00689972 · Cited by 32 · see citing works
Chen, P. B., Davern, L. B., Katz, J., Eldridge, J. H., & Michalek, S. M. (1996) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1996.tb00181.x · Cited by 29 · see citing works
Lee, J. K., & Pierce, M. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.1312 · Cited by 19 · see citing works
Wagner, S., Enss, M., Cornberg, M., Mix, H., Schumann, S., Kirchner, G. I., Jähne, J., Manns, M. P., & Beil, W. (1998) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050717 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pseudomonas aeruginosa Biofilms
Thi, M. T. T., Wibowo, D., & Rehm, B. H. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228671 · Cited by 923 · see citing works
From in vitro to in vivo Models of Bacterial Biofilm-Related Infections
Lebeaux, D., Chauhan, A., Rendueles, O., & Beloin, C. (2013) · Pathogens · doi:10.3390/pathogens2020288 · Cited by 551 · see citing works
Interactions in multispecies biofilms: do they actually matter?
Burmølle, M., Ren, D., Bjarnsholt, T., & Sørensen, S. J. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2013.12.004 · Cited by 544 · 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
Filkins, L., Graber, J. A., Olson, D. G., Dolben, E. L., Lynd, L. R., Bhuju, S., & O’Toole, G. A. (2015) · Journal of Bacteriology · doi:10.1128/jb.00059-15 · Cited by 342 · 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-citationHajishengallis, G., & Lamont, R. J. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.02.010 · Cited by 275 · see citing works
In vivo and In vitro Interactions between Pseudomonas aeruginosa and Staphylococcus spp.
Hotterbeekx, A., Kumar‐Singh, S., Goossens, H., & Malhotra‐Kumar, S. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00106 · Cited by 265 · see citing works
Peptidoglycan Muropeptides: Release, Perception, and Functions as Signaling Molecules
Irazoki, O., Hernández, S. B., & Cava, F. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00500 · Cited by 200 · see citing works
Mechanisms of synergy in polymicrobial infections
Murray, J. L., Connell, J. L., Stacy, A., Turner, K. H., & Whiteley, M. (2014) · The Journal of Microbiology · doi:10.1007/s12275-014-4067-3 · Cited by 201 · see citing works
Self-citationTwo-component systems required for virulence in Pseudomonas aeruginosa
Francis, V. I., Stevenson, E. C., & Porter, S. L. (2017) · FEMS Microbiology Letters · doi:10.1093/femsle/fnx104 · Cited by 192 · see citing works
Bacterial fight-and-flight responses enhance virulence in a polymicrobial infection
Stacy, A., Everett, J., Jorth, P., Trivedi, U., Rumbaugh, K. P., & Whiteley, M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400586111 · Cited by 192 · see citing works
Self-citation“It Takes a Village”: Mechanisms Underlying Antimicrobial Recalcitrance of Polymicrobial Biofilms
Orazi, G., & O’Toole, G. A. (2019) · Journal of Bacteriology · doi:10.1128/jb.00530-19 · Cited by 184 · 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-citationPseudomonas aeruginosa biofilms and their partners in crime
Cendra, M. D. M., & Torrents, E. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107734 · Cited by 179 · see citing works
Limoli, D. H., Whitfield, G. B., Kitao, T., Ivey, M. L., Davis, M. R., Grahl, N., Hogan, D. A., Rahme, L. G., Howell, P. L., O’Toole, G. A., et al. (2017) · mBio · doi:10.1128/mbio.00186-17 · Cited by 172 · see citing works
Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa
LeRoux, M., Kirkpatrick, R. L., Montauti, E. I., Tran, B. Q., Peterson, S. B., Harding, B. N., Whitney, J. C. C., Russell, A. B., Traxler, B. A., Goo, Y. A., et al. (2015) · eLife · doi:10.7554/elife.05701 · Cited by 158 · see citing works
Pathogens 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
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
Self-citationThe manifold roles of microbial ribosomal peptide–based natural products in physiology and ecology
Li, Y., & Rebuffat, S. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.006545 · Cited by 148 · see citing works
Polybacterial human disease: the ills of social networking
Short, F. L., Murdoch, S. L., & Ryan, R. P. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2014.05.007 · Cited by 141 · see citing works
In vitro and ex vivo systems at the forefront of infection modeling and drug discovery
Shi, D., Mi, G., Wang, M., & Webster, T. J. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.10.030 · Cited by 141 · see citing works
Biofilm Bacteria Use Stress Responses to Detect and Respond to Competitors
Lories, B., Roberfroid, S., Dieltjens, L., Coster, D. D., Foster, K. R., & Steenackers, H. P. L. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.065 · Cited by 137 · see citing works
Coulter, L. B., McLean, R. J. C., Rohde, R. E., & Aron, G. M. (2014) · Viruses · doi:10.3390/v6103778 · Cited by 129 · see citing works
Polymicrobial–Host Interactions during Infection
Tay, W. H., Chong, K. K. L., & Kline, K. A. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.05.006 · Cited by 126 · see citing works
Limoli, D. H., & Hoffman, L. R. (2019) · Thorax · doi:10.1136/thoraxjnl-2018-212616 · Cited by 130 · see citing works
Bacterial Community Interactions During Chronic Respiratory Disease
Welp, A. L., & Bomberger, J. M. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00213 · Cited by 127 · see citing works
Nguyen, A. T., & Oglesby, A. G. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7596-3 · Cited by 123 · see citing works
Response of host–bacterial colonization in shrimp to developmental stage, environment and disease
Xiong, J., Dai, W., Qiu, Q., Zhu, J., Yang, W., & Li, C. (2018) · Molecular Ecology · doi:10.1111/mec.14822 · Cited by 123 · see citing works
Whiteson, K., Bailey, B., Bergkessel, M., Conrad, D., Delhaès, L., Felts, B., Harris, J. K., Hunter, R. C., Lim, Y. W., Maughan, H., et al. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201312-2129pp · Cited by 122 · see citing works
O’Brien, S., & Fothergill, J. L. (2017) · FEMS Microbiology Letters · doi:10.1093/femsle/fnx128 · Cited by 118 · see citing works
Staphylococcus aureus α toxin potentiates opportunistic bacterial lung infections
Cohen, T. S., Hilliard, J. J., Jones-Nelson, O., Keller, A. E., O’Day, T. L., Tkaczyk, C., DiGiandomenico, A., Hamilton, M. M., Pelletier, M. R., Wang, Q., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad9922 · Cited by 118 · see citing works
Cuthbertson, L., Rogers, G. B., Walker, A. W., Oliver, A., Green, L. E., Daniels, T. W. V., Carroll, M. P., Parkhill, J., Bruce, K. D., & Gast, C. (2015) · The ISME Journal · doi:10.1038/ismej.2015.198 · Cited by 114 · see citing works
Ibberson, C. B., Stacy, A., Fleming, D. F., Dees, J. L., Rumbaugh, K. P., Gilmore, M. S., & Whiteley, M. (2017) · Nature Microbiology · doi:10.1038/nmicrobiol.2017.79 · Cited by 114 · see citing works
Self-citationBriaud, P., Camus, L., Bastien, S., Doléans-Jordheim, A., Vandenesch, F., & Moreau, K. (2019) · Scientific Reports · doi:10.1038/s41598-019-52975-z · Cited by 106 · see citing works
Community interactions and spatial structure shape selection on antibiotic resistant lineages
Estrela, S., & Brown, S. P. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006179 · Cited by 103 · see citing works
Human skin commensals augment Staphylococcus aureus pathogenesis
Boldock, E., Surewaard, B. G. J., Shamarina, D., Na, M., Fei, Y., Ali, A. M., Williams, A., Pollitt, E. J. G., Szkuta, P. T., Morris, P., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0198-3 · Cited by 103 · see citing works
Xu, Z., Xie, J., Soteyome, T., Peters, B. M., Shirtliff, M. E., Liu, J., & Harro, J. M. (2019) · Current Opinion in Food Science · doi:10.1016/j.cofs.2019.03.006 · Cited by 101 · see citing works
Mucins trigger dispersal of Pseudomonas aeruginosa biofilms
Co, J. Y., Cárcamo‐Oyarce, G., Billings, N., Wheeler, K. M., Grindy, S. C., Holten‐Andersen, N., & Ribbeck, K. (2018) · npj Biofilms and Microbiomes · doi:10.1038/s41522-018-0067-0 · Cited by 91 · see citing works
Michelsen, C. F., Khademi, S. M. H., Johansen, H. K., Ingmer, H., Dorrestein, P. C., & Jelsbak, L. (2015) · The ISME Journal · doi:10.1038/ismej.2015.220 · Cited by 92 · see citing works
A Commensal Bacterium Promotes Virulence of an Opportunistic Pathogen via Cross-Respiration
Stacy, A., Fleming, D. F., Lamont, R. J., Rumbaugh, K. P., & Whiteley, M. (2016) · mBio · doi:10.1128/mbio.00782-16 · Cited by 93 · see citing works
Self-citationPolymicrobial 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
Reece, E., Doyle, S., Greally, P., Renwick, J. A. A., & McClean, S. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01205 · Cited by 91 · see citing works
Rapid diversification of Pseudomonas aeruginosa in cystic fibrosis lung-like conditions
Schick, A., & Kassen, R. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1721270115 · Cited by 88 · see citing works
Molecular Mechanisms of Staphylococcus and Pseudomonas Interactions in Cystic Fibrosis
Biswas, L., & Götz, F. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.824042 · Cited by 89 · see citing works
Iron depletion enhances production of antimicrobials by Pseudomonas aeruginosa
Nguyen, A. T., Jones, J. W., Ruge, M. A., Kane, M. A., & Oglesby-Sherrouse, A. G. (2015) · Journal of Bacteriology · doi:10.1128/jb.00072-15 · Cited by 88 · see citing works
Trizna, E. Y., Yarullina, M. N., Baidamshina, D. R., Миронова, А. В., Akhatova, F. S., Rozhina, E. V., Fakhrullin, R. F., Мунавировна, Х. А., Рафаэловна, К. А., Bogachev, M. I., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-71834-w · Cited by 92 · see citing works
Impact of polymicrobial biofilms in catheter-associated urinary tract infections
Azevedo, A. S., Almeida, C., Melo, L. F., & Azevedo, N. F. (2016) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2016.1240656 · Cited by 87 · see citing works
Yung, D. B. Y., Sircombe, K. J., & Pletzer, D. (2021) · Molecular Microbiology · doi:10.1111/mmi.14699 · Cited by 86 · see citing works
Mechanisms of Pyocyanin Toxicity and Genetic Determinants of Resistance in Staphylococcus aureus
Noto, M. J., Burns, W. J., Beavers, W. N., & Skaar, E. P. (2017) · Journal of Bacteriology · doi:10.1128/jb.00221-17 · Cited by 85 · see citing works
Mirani, Z. A., Fatima, A., Urooj, S., Aziz, M., Khan, M. N., & Abbas, T. (2018) · Europe PMC (PubMed Central) · doi:10.22038/ijbms.2018.28525.6917 · Cited by 85 · see citing works
Bacterial Interactions in the Context of Chronic Wound Biofilm: A Review
Durand, B. A. R. N., Pouget, C., Magnan, C., Molle, V., Lavigne, J., & Dunyach‐Remy, C. (2022) · Microorganisms · doi:10.3390/microorganisms10081500 · Cited by 85 · see citing works
Dworkin, J. E. (2014) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091213-112844 · Cited by 79 · see citing works
Michelsen, C. F., Christensen, A.-M. J., Bojer, M. S., Høiby, N., Ingmer, H., & Jelsbak, L. (2014) · Journal of Bacteriology · doi:10.1128/jb.02006-14 · Cited by 80 · see citing works
Jin, K., Zhou, L., Jiang, H., Sun, S., Fang, Y.-L., Liu, J., Zhang, X., & He, Y. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.09.003 · Cited by 79 · see citing works
Human pathogenic bacteria, fungi, and viruses inDrosophila
Panayidou, S., Ioannidou, E., & Apidianakis, Y. (2014) · Virulence · doi:10.4161/viru.27524 · Cited by 79 · see citing works
Strain- and Substrate-Dependent Redox Mediator and Electricity Production by Pseudomonas aeruginosa
Bosire, E. M., Blank, L. M., & Rosenbaum, M. A. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01342-16 · Cited by 77 · see citing works
Interpreting infective microbiota: the importance of an ecological perspective
Rogers, G. B., Hoffman, L. R., Carroll, M. P., & Bruce, K. D. (2013) · Trends in Microbiology · doi:10.1016/j.tim.2013.03.004 · Cited by 76 · see citing works
Liu, W., Russel, J., Røder, H. L., Madsen, J. S., Burmølle, M., & Sørensen, S. J. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13816 · Cited by 74 · see citing works
Albumin Inhibits Pseudomonas aeruginosa Quorum Sensing and Alters Polymicrobial Interactions
Smith, A. C., Rice, A. M., Sutton, B., Gabrilska, R. A., Wessel, A. K., Whiteley, M., & Rumbaugh, K. P. (2017) · Infection and Immunity · doi:10.1128/iai.00116-17 · Cited by 74 · see citing works
Self-citationSmall Is Mighty—Chemical Communication Systems inPseudomonas aeruginosa
Ahator, S. D., & Zhang, L. (2019) · Annual Review of Microbiology · doi:10.1146/annurev-micro-020518-120044 · Cited by 73 · 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-citationCava, F., & de Pedro, M. A. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.01.004 · Cited by 70 · see citing works
Moriarty, T. F., Grainger, D. W., & Richards, R. G. (2014) · European Cells and Materials · doi:10.22203/ecm.v028a09 · Cited by 70 · see citing works
Schafhauser, J., Lepine, F. L., McKay, G. A., Ahlgren, H. G., Khakimova, M., & Nguyen, D. M. (2014) · Journal of Bacteriology · doi:10.1128/jb.01086-13 · Cited by 69 · see citing works
Gilmore, S. A., Naseem, S., Konopka, J. B., & Sil, A. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003799 · Cited by 68 · see citing works
Bernardy, E. E., Petit, R. A., Raghuram, V., Alexander, A. M., Read, T. D., & Goldberg, J. B. (2020) · mBio · doi:10.1128/mbio.00735-20 · Cited by 67 · see citing works
Maan, H., Itkin, M., Malitsky, S., Friedman, J., & Kolodkin‐Gal, I. (2022) · Nature Communications · doi:10.1038/s41467-021-27904-2 · Cited by 63 · see citing works
Djapgne, L., Panja, S., Brewer, L. K., Gans, J. H., Kane, M. A., Woodson, S. A., & Oglesby, A. G. (2018) · Journal of Bacteriology · doi:10.1128/jb.00704-17 · Cited by 63 · see citing works
Cooperation and Conflict Within the Microbiota and Their Effects On Animal Hosts
Figueiredo, A. R. T., & Kramer, J. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2020.00132 · Cited by 61 · see citing works
Sensing Gram-negative bacteria: a phylogenetic perspective
Neyen, C. D., & Lemaître, B. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.10.007 · Cited by 61 · see citing works
Scoffield, J. A., Duan, D., Zhu, F., & Wu, H. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006300 · Cited by 57 · see citing works
Hu, Y. H., Niu, Y., Ye, X., Zhu, C., Tong, T., Zhou, Y., Zhou, X., Cheng, L., & Ren, B. (2021) · Pathogens · doi:10.3390/pathogens10081036 · Cited by 57 · see citing works
Lee, K., Lee, K., Kim, D.-G., & Yoon, S. S. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.01182-17 · Cited by 58 · see citing works
Multifactorial Competition and Resistance in a Two-Species Bacterial System
Khare, A., & Tavazoie, S. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005715 · Cited by 58 · see citing works
Ward, A. C., Connolly, P., & Tucker, N. P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091732 · Cited by 57 · see citing works
Bacterial multispecies studies and microbiome analysis of a plant disease
da Silva, D. P., Castañeda‐Ojeda, M. P., Moretti, C., Buonaurio, R., Ramos, C., & Venturi, V. (2014) · Microbiology · doi:10.1099/mic.0.074468-0 · Cited by 56 · see citing works
Wilkinson, H. N., Iveson, S., Catherall, P., & Hardman, M. J. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01450 · Cited by 56 · see citing works
Reece, E., Bettio, P. H. D. A., & Renwick, J. (2021) · Antibiotics · doi:10.3390/antibiotics10070827 · Cited by 51 · see citing works
Antimicrobial resistance three ways: healthcare crisis, major concepts and the relevance of biofilms
Jorge, P., Magalhães, A. P., Grainha, T., Alves, D. F., Sousa, A. M., Lopes, S. P., & Pereira, M. O. (2019) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiz115 · Cited by 56 · see citing works
Christofi, T., Panayidou, S., Dieronitou, I., Michael, C., & Apidianakis, Y. (2019) · Scientific Reports · doi:10.1038/s41598-019-51058-3 · Cited by 54 · see citing works
Park, H., McGill, S. L., Arnold, A. D., & Carlson, R. P. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03377-x · Cited by 54 · see citing works
Hoffman, C. L., Lalsiamthara, J., & Aballay, A. (2020) · mBio · doi:10.1128/mbio.00060-20 · Cited by 54 · see citing works
Advances in understanding Pseudomonas
Tümmler, B., Wiehlmann, L., Klockgether, J., & Cramer, N. (2014) · F1000Prime Reports · doi:10.12703/p6-9 · Cited by 53 · see citing works
Cooperative secretions facilitate host range expansion in bacteria
McNally, L., Viana, M. S., & Brown, S. P. (2014) · Nature Communications · doi:10.1038/ncomms5594 · Cited by 53 · see citing works
Wright, C. J., Xue, P., Hirano, T., Liu, C., Whitmore, S. E., Hackett, M., & Lamont, R. J. (2014) · MicrobiologyOpen · doi:10.1002/mbo3.177 · Cited by 53 · see citing works
Antibiotics and the art of bacterial war
Cornforth, D. M., & Foster, K. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513608112 · Cited by 53 · see citing works
Kvich, L., Burmølle, M., Bjarnsholt, T., & Lichtenberg, M. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00396 · Cited by 52 · see citing works
Coinfection with Pseudomonas aeruginosa and Aspergillus fumigatus in cystic fibrosis
Keown, K., Reid, A. J. M., Moore, J. E., Taggart, C. C., & Downey, D. G. (2020) · European Respiratory Review · doi:10.1183/16000617.0011-2020 · Cited by 51 · see citing works
Barraza, J. P., & Whiteley, M. (2021) · mBio · doi:10.1128/mbio.00047-21 · Cited by 47 · see citing works
Self-citationAlavi, M., Antonic, V., Stojadinovic, A., Zhang, B., & Izadjoo, M. J. (2013) · Infection and Drug Resistance · doi:10.2147/idr.s49039 · Cited by 52 · see citing works
Guillaume, O., Butnarasu, C., Visentin, S., & Reimhult, E. (2022) · Biofilm · doi:10.1016/j.bioflm.2022.100089 · Cited by 51 · see citing works
N-acetylglucosamine Regulates Virulence Properties in Microbial Pathogens
Naseem, S., & Konopka, J. B. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004947 · Cited by 51 · see citing works
Meirelles, L. A., Perry, E. K., Bergkessel, M., & Newman, D. K. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001093 · Cited by 49 · see citing works
Microbial Interplay in Skin and Chronic Wounds
Sachdeva, C., Satyamoorthy, K., & Murali, T. S. (2022) · Current Clinical Microbiology Reports · doi:10.1007/s40588-022-00180-4 · Cited by 52 · see citing works
Ibberson, C. B., Barraza, J. P., Holmes, A. L., Cao, P., & Whiteley, M. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212340119 · Cited by 46 · see citing works
Self-citationValentini, T., Lucas, S. K., Binder, K. A., Cameron, L. C., Motl, J. A., Dunitz, J., & Hunter, R. C. (2020) · Nature Communications · doi:10.1038/s41467-020-16163-2 · Cited by 48 · see citing works
Mumford, R., & Friman, V. (2016) · Evolutionary Applications · doi:10.1111/eva.12435 · Cited by 47 · see citing works
Simoska, O., Sans, M., Eberlin, L. S., Shear, J. B., & Stevenson, K. J. (2019) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2019.111538 · Cited by 47 · see citing works
Mohan, R., Sanpitakseree, C., Desai, A. V., Sevgen, S. E., Schroeder, C. M., & Kenis, P. J. A. (2015) · RSC Advances · doi:10.1039/c5ra04092b · Cited by 46 · see citing works
- Authors
- Korgaonkar, A., 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
- 2012-12-31
- Volume
- 110
- Issue
- 3
- Pages
- 1059-1064
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3549110
- OpenAlex
- W2062817953
- Cited by
- 315
- References
- 59
- Citations by year
- 2026: 14 · 2025: 24 · 2024: 16 · 2023: 27 · 2022: 26 · 2021: 23 · 2020: 24 · 2019: 26 · 2018: 21 · 2017: 21 · 2016: 24 · 2015: 32 · 2014: 28 · 2013: 9
- FWCI
- 8.88
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI075068)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Keywords
- Pseudomonas aeruginosa, co-infection, bacterial synergy, peptidoglycan sensing, Gram-positive bacteria, extracellular virulence factors, lytic activity, community-based surveillance
- MeSH terms
- Animals, Base Sequence, Disease Models, Animal, DNA, Bacterial, Drosophila melanogaster, Female, Genes, Bacterial, Humans, Male, Mutation, Peptidoglycan, Pseudomonas aeruginosa, Pseudomonas Infections, Staphylococcal Infections, Staphylococcus aureus, Virulence, Mice, 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