Abstract
Pseudomonas aeruginosa is a robust and versatile organism capable of surviving and prospering in a diverse array of environments and is an opportunistic pathogen of humans. One reason for the success of this pathogen is the large arsenal of antimicrobial weapons that it possesses. Here we focus our attention on these antimicrobial weapons and how they give P. aeruginosa a survival edge in polymicrobial environments. We define antimicrobial weapons as components produced by P. aeruginosa that are used to kill, inhibit growth and/or subvert key cellular functions in other microbes. P. aeruginosa has a large and complex genome and encodes an armament of antimicrobial weapons that fall into two subclasses; those that are delivered directly to competing microbes using a contact-dependent method, and those that are secreted in a contact-independent manner into the environment to then be available to target neighbouring cells. This chapter provides an overview of the major antimicrobial weapons possessed by P. aeruginosa, captures recent advances in the field and discusses how these could be targeted as a therapeutic intervention, or potentially harnessed to combat infection.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Abdel-Mawgoud AM, Lépine F, Déziel E (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86:1323–1336. https://doi.org/10.1007/s00253-010-2498-2
Adler C, Corbalán NS, Seyedsayamdost MR et al (2012) Catecholate siderophores protect bacteria from pyochelin toxicity. PLoS One 7:e46754. https://doi.org/10.1371/journal.pone.0046754
Ahmad S, Wang B, Walker MD et al (2019) An interbacterial toxin inhibits target cell growth by synthesizing (p)ppApp. Nature 575:674–678. https://doi.org/10.1038/s41586-019-1735-9
Allen JP, Hauser AR (2019) Diversity of contact-dependent growth inhibition systems of Pseudomonas aeruginosa. J Bacteriol 201:1–12. https://doi.org/10.1128/JB.00776-18
Allen JP, Ozer EA, Minasov G et al (2020) A comparative genomics approach identifies contact-dependent growth inhibition as a virulence determinant. Proc Natl Acad Sci U S A 117:6811–6821. https://doi.org/10.1073/pnas.1919198117
Allsopp LP, Wood TE, Howard SA et al (2017) RsmA and AmrZ orchestrate the assembly of all three type VI secretion systems in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 114:7707–7712. https://doi.org/10.1073/pnas.1700286114
Allsopp LP, Bernal P, Nolan LM, Filloux A (2020) Causalities of war: the connection between type VI secretion system and microbiota. Cell Microbiol 22:e13153. https://doi.org/10.1111/cmi.13153
Andersen SR, Bjune G, Lyngby J et al (1995) Short-chain lipopolysaccharide mutants of serogroup B Neisseria meningitidis of potential value for production of outer membrane vesicle vaccines. Microb Pathog 19:159–168. https://doi.org/10.1006/mpat.1995.0054
Anderson MS, Garcia EC, Cotter PA (2012) The Burkholderia bcpAIOB genes define unique classes of two-partner secretion and contact dependent growth inhibition systems. PLoS Genet 8:e1002877. https://doi.org/10.1371/journal.pgen.1002877
Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. https://doi.org/10.1016/S0168-6445(03)00055-X
Ankenbauer RG, Quan HN (1994) FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J Bacteriol 176:307–319. https://doi.org/10.1128/jb.176.2.307-319.1994
Aoki SK, Pamma R, Hernday AD et al (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309:1245–1248. https://doi.org/10.1126/science.1115109
Aoki SK, Diner EJ, de Roodenbeke CT et al (2010) A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468:439–442. https://doi.org/10.1038/nature09490
Bara JJ, Matson Z, Remold SK (2018) Life in the cystic fibrosis upper respiratory tract influences competitive ability of the opportunistic pathogen Pseudomonas aeruginosa. R Soc Open Sci 5:1–13. https://doi.org/10.1098/rsos.180623
Barequet IS, Ben Simon GJ, Safrin M et al (2004) Pseudomonas aeruginosa LasA protease in treatment of experimental staphylococcal keratitis. Antimicrob Agents Chemother 48:1681–1687. https://doi.org/10.1128/AAC.48.5.1681-1687.2004
Baron SS, Rowe JJ (1981) Antibiotic action of pyocyanin. Antimicrob Agents Chemother 20:814–820. https://doi.org/10.1128/aac.20.6.814
Baron SS, Terranova G, Rowe JJ (1989) Molecular mechanism of the antimicrobial action of pyocyanin. Curr Microbiol 18:223–230. https://doi.org/10.1007/BF01570296
Barreteau H, Bouhss A, Fourgeaud M et al (2009) Human- and plant-pathogenic Pseudomonas species produce bacteriocins exhibiting colicin M-like hydrolase activity towards peptidoglycan precursors. J Bacteriol 191:3657–3664. https://doi.org/10.1128/JB.01824-08
Basler M, Mekalanos JJ (2012) Type 6 secretion dynamics within and between bacterial cells. Science 337:815. https://doi.org/10.1126/science.1222901
Basler M, Pilhofer M, Henderson GP et al (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182–186. https://doi.org/10.1038/nature10846
Basler M, Ho BT, Mekalanos JJ (2013) Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152:884–894. https://doi.org/10.1016/j.cell.2013.01.042
Baysse C, Meyer JM, Plesiat P et al (1999) Uptake of pyocin S3 occurs through the outer membrane ferripyoverdine type II receptor of Pseudomonas aeruginosa. J Bacteriol 181:3849–3851. https://doi.org/10.1128/JB.181.12.3849-3851.1999
Beck CM, Willett JLE, Cunningham DA et al (2016) CdiA effectors from uropathogenic Escherichia coli use heterotrimeric osmoporins as receptors to recognize target bacteria. PLoS Pathog 12:e1005925. https://doi.org/10.1371/journal.ppat.1005925
Benincasa M, Abalos A, Oliveira I, Manresa A (2004) Chemical structure, surface properties and biological activities of the biosurfactant produced by Pseudomonas aeruginosa LBI from soapstock. Antonie Van Leeuwenhoek 85:1–8. https://doi.org/10.1023/B:ANTO.0000020148.45523.41
Bergan T, Ekströn B, Nord CE (1986) Ecological impacts of antibacterial agents: Stockholm, March 7–8, 1986. Scand J Infect Dis 18:1–203. https://doi.org/10.3109/inf.1986.18.suppl-49.01
Bernal P, Furniss RCD, Fecht S et al (2021) A novel stabilization mechanism for the type VI secretion system sheath. Proc Natl Acad Sci U S A 118:e2008500118. https://doi.org/10.1073/pnas.2008500118
Berni B, Soscia C, Djermoun S et al (2019) A type VI secretion system trans-kingdom effector is required for the delivery of a novel antibacterial toxin in Pseudomonas aeruginosa. Front Microbiol 10:1218. https://doi.org/10.3389/fmicb.2019.01218
Beveridge TJ (1999) Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733. https://doi.org/10.1128/JB.181.16.4725-4733.1999
Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z (1997) Interactions between biofilms and the environment. FEMS Microbiol Rev 20:291–303. https://doi.org/10.1111/j.1574-6976.1997.tb00315.x
Bingle LE, Bailey CM, Pallen MJ (2008) Type VI secretion: a beginner’s guide. Curr Opin Microbiol 11:3–8. https://doi.org/10.1016/j.mib.2008.01.006
Bladergroen MR, Badelt K, Spaink HP (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16:53–64. https://doi.org/10.1094/MPMI.2003.16.1.53
Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173:170–177. https://doi.org/10.1007/s002039900127
Bottery MJ, Passaris I, Dytham C et al (2019) Spatial organization of expanding bacterial colonies is affected by contact-dependent growth inhibition. Curr Biol 29:3622–3634.e5. https://doi.org/10.1016/j.cub.2019.08.074
Brandel J, Humbert N, Elhabiri M et al (2012) Pyochelin, a siderophore of Pseudomonas aeruginosa: physicochemical characterization of the iron(III), copper(II) and zinc(II) complexes. Dalton Trans 41:2820–2834. https://doi.org/10.1039/c1dt11804h
Braun P, de Groot A, Bitter W, Tommassen J (1998) Secretion of elastinolytic enzymes and their propeptides by Pseudomonas aeruginosa. J Bacteriol 180:3467–3469. https://doi.org/10.1128/JB.180.13.3467-3469.1998
Brazas MD, Hancock REW (2005) Ciprofloxacin induction of a susceptibility determinant in Pseudomonas aeruginosa. Antimicrob Agents Chemother 49:3222–3227. https://doi.org/10.1128/AAC.49.8.3222-3227.2005
Burkinshaw BJ, Liang X, Wong M et al (2018) A type VI secretion system effector delivery mechanism dependent on PAAR and a chaperone-co-chaperone complex. Nat Microbiol 3:632–640. https://doi.org/10.1038/s41564-018-0144-4
Calfee MW, Coleman JP, Pesci EC (2001) Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 98:11633–11637. https://doi.org/10.1073/pnas.201328498
Carterson AJ, Morici LA, Jackson DW et al (2004) The transcriptional regulator AlgR controls cyanide production in Pseudomonas aeruginosa. J Bacteriol 186:6837–6844. https://doi.org/10.1128/JB.186.20.6837-6844.2004
Caruana JC, Walper SA (2020) Bacterial membrane vesicles as mediators of microbe - microbe and microbe - host community interactions. Front Microbiol 11:432. https://doi.org/10.3389/fmicb.2020.00432
Cassat JE, Skaar EP (2013) Iron in infection and immunity. Cell Host Microbe 13:509–519. https://doi.org/10.1016/j.chom.2013.04.010
Castric PA (1975) Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21:613–618. https://doi.org/10.1139/m75-088
Chang W, Small DA, Toghrol F, Bentley WE (2005) Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics 6:115. https://doi.org/10.1186/1471-2164-6-115
Cherrak Y, Filella-Merce I, Schmidt V et al (2021) Inhibiting type VI secretion system activity with a biomimetic peptide designed to target the baseplate wedge complex. MBio 12:e0134821. https://doi.org/10.1128/mBio.01348-21
Choi D-S, Kim D-K, Choi SJ et al (2011) Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics 11:3424–3429. https://doi.org/10.1002/pmic.201000212
Chrzanowski Ł, Ławniczak Ł, Czaczyk K (2012) Why do microorganisms produce rhamnolipids? World J Microbiol Biotechnol 28:401–419. https://doi.org/10.1007/s11274-011-0854-8
Cipollone R, Bigotti MG, Frangipani E et al (2004) Characterization of a rhodanese from the cyanogenic bacterium Pseudomonas aeruginosa. Biochem Biophys Res Commun 325:85–90. https://doi.org/10.1016/j.bbrc.2004.09.214
Cooper M, Tavankar GR, Williams HD (2003) Regulation of expression of the cyanide-insensitive terminal oxidase in Pseudomonas aeruginosa. Microbiology (Reading, Engl) 149:1275–1284. https://doi.org/10.1099/mic.0.26017-0
Costa TRD, Felisberto-Rodrigues C, Meir A et al (2015) Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359. https://doi.org/10.1038/nrmicro3456
Cox CD (1980) Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol 142:581–587. https://doi.org/10.1128/jb.142.2.581-587.1980
Cox CD, Adams P (1985) Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun 48:130–138. https://doi.org/10.1128/iai.48.1.130-138.1985
Cunningham L, Pitt M, Williams HD (1997) The cioAB genes from Pseudomonas aeruginosa code for a novel cyanide-insensitive terminal oxidase related to the cytochrome bd quinol oxidases. Mol Microbiol 24:579–591. https://doi.org/10.1046/j.1365-2958.1997.3561728.x
Cunrath O, Graulier G, Carballido-Lopez A et al (2020) The pathogen Pseudomonas aeruginosa optimizes the production of the siderophore pyochelin upon environmental challenges. Metallomics 12:2108–2120. https://doi.org/10.1039/d0mt00029a
Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036. https://doi.org/10.1128/JB.185.3.1027-1036.2003
de Araujo LV, Abreu F, Lins U et al (2011) Rhamnolipid and surfactin inhibit Listeria monocytogenes adhesion. Food Res Int 44:481–488. https://doi.org/10.1016/j.foodres.2010.09.002
Denayer S, Matthijs S, Cornelis P (2007) Pyocin S2 (Sa) kills Pseudomonas aeruginosa strains via the FpvA type I ferripyoverdine receptor. J Bacteriol 189:7663–7668. https://doi.org/10.1128/JB.00992-07
Dharni S, Alam M, Kalani K et al (2012) Production, purification, and characterization of antifungal metabolite from Pseudomonas aeruginosa SD12, a new strain obtained from tannery waste polluted soil. J Microbiol Biotechnol 22:674–683. https://doi.org/10.4014/jmb.1109.09061
Dharni S, Sanchita SA et al (2014) The interaction pattern between a homology model of 40S ribosomal S9 protein of Rhizoctonia solani and 1-hydroxyphenaize by docking study. Biomed Res Int 2014:682946. https://doi.org/10.1155/2014/682946
Dingemans J, Ghequire MGK, Craggs M et al (2016) Identification and functional analysis of a bacteriocin, pyocin S6, with ribonuclease activity from a Pseudomonas aeruginosa cystic fibrosis clinical isolate. Microbiologyopen 5:413–423. https://doi.org/10.1002/mbo3.339
Dorosky RJ, Yu JM, Pierson LS, Pierson EA (2017) Pseudomonas chlororaphis produces two distinct R-tailocins that contribute to bacterial competition in biofilms and on roots. Appl Environ Microbiol 83:e00706–e00717. https://doi.org/10.1128/AEM.00706-17
Duport C, Baysse C, Michel-Briand Y (1995) Molecular characterization of pyocin S3, a novel S-type pyocin from Pseudomonas aeruginosa. J Biol Chem 270:8920–8927. https://doi.org/10.1074/jbc.270.15.8920
Dusane DH, Nancharaiah YV, Zinjarde SS, Venugopalan VP (2010) Rhamnolipid mediated disruption of marine Bacillus pumilus biofilms. Colloids Surf B Biointerfaces 81:242–248. https://doi.org/10.1016/j.colsurfb.2010.07.013
Elfarash A, Wei Q, Cornelis P (2012) The soluble pyocins S2 and S4 from Pseudomonas aeruginosa bind to the same FpvAI receptor. Microbiologyopen 1:268–275. https://doi.org/10.1002/mbo3.27
Elfarash A, Dingemans J, Ye L et al (2014) Pore-forming pyocin S5 utilizes the FptA ferripyochelin receptor to kill Pseudomonas aeruginosa. Microbiology (Reading, Engl) 160:261–269. https://doi.org/10.1099/mic.0.070672-0
Emmerich R, Löw O (1899) Bakteriolytische Enzyme als Ursache der erworbenen Immunität und die Heilung von Infectionskrankheiten durch dieselben. Zeitschr f Hygiene 31:1–65. https://doi.org/10.1007/BF02206499
Fan E, Chauhan N, Udatha DBRKG et al (2016) Type V secretion systems in bacteria. Microbiol Spectr 4:1–24. https://doi.org/10.1128/microbiolspec.VMBF-0009-2015
Filiatrault MJ, Munson RS, Campagnari AA (2001) Genetic analysis of a pyocin-resistant lipooligosaccharide (LOS) mutant of Haemophilus ducreyi: restoration of full-length LOS restores pyocin sensitivity. J Bacteriol 183:5756–5761. https://doi.org/10.1128/JB.183.19.5756-5761.2001
Fontoura R, Spada JC, Silveira ST et al (2009) Purification and characterization of an antimicrobial peptide produced by Pseudomonas sp. strain 4B. World J Microbiol Biotechnol 25:205–213. https://doi.org/10.1007/s11274-008-9882-4
France MT, Remold SK (2016) Interference competition among household strains of pseudomonas. Microb Ecol 72:821–830. https://doi.org/10.1007/s00248-015-0652-1
Frangipani E, Pérez-Martínez I, Williams HD et al (2014) A novel cyanide-inducible gene cluster helps protect Pseudomonas aeruginosa from cyanide. Environ Microbiol Rep 6:28–34. https://doi.org/10.1111/1758-2229.12105
Fraser A, Prokhorov NS, Jiao F et al (2021) Quantitative description of a contractile macromolecular machine. Sci Adv 7:eabf9601. https://doi.org/10.1126/sciadv.abf9601
Fyfe JA, Harris G, Govan JR (1984) Revised pyocin ty** method for Pseudomonas aeruginosa. J Clin Microbiol 20:47–50. https://doi.org/10.1128/jcm.20.1.47-50.1984
Gambello MJ, Iglewski BH (1991) Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 173:3000–3009. https://doi.org/10.1128/jb.173.9.3000-3009.1991
Garcia EC, Anderson MS, Hagar JA, Cotter PA (2013) Burkholderia BcpA mediates biofilm formation independently of interbacterial contact-dependent growth inhibition. Mol Microbiol 89:1213–1225. https://doi.org/10.1111/mmi.12339
Garcia EC, Perault AI, Marlatt SA, Cotter PA (2016) Interbacterial signaling via Burkholderia contact-dependent growth inhibition system proteins. Proc Natl Acad Sci U S A 113:8296–8301. https://doi.org/10.1073/pnas.1606323113
Gebhart D, Lok S, Clare S et al (2015) A modified R-type bacteriocin specifically targeting Clostridium difficile prevents colonization of mice without affecting gut microbiota diversity. MBio 6:e02368–e02314. https://doi.org/10.1128/mBio.02368-14
Geske GD, O’Neill JC, Blackwell HE (2008) Expanding dialogues: from natural autoinducers to non-natural analogues that modulate quorum sensing in Gram-negative bacteria. Chem Soc Rev 37:1432–1447. https://doi.org/10.1039/b703021p
Ghequire MGK, De Mot R (2015) The tailocin tale: peeling off phage tails. Trends Microbiol 23:587–590. https://doi.org/10.1016/j.tim.2015.07.011
Ghequire MGK, Öztürk B (2018) A colicin M-type bacteriocin from Pseudomonas aeruginosa targeting the HxuC heme receptor requires a novel immunity partner. Appl Environ Microbiol 84:00716–00718. https://doi.org/10.1128/AEM.00716-18
Ghequire MGK, Garcia-Pino A, Lebbe EKM et al (2013) Structural determinants for activity and specificity of the bacterial toxin LlpA. PLoS Pathog 9:e1003199. https://doi.org/10.1371/journal.ppat.1003199
Ghequire MGK, Dingemans J, Pirnay J-P et al (2014) O serotype-independent susceptibility of Pseudomonas aeruginosa to lectin-like pyocins. Microbiologyopen 3:875–884. https://doi.org/10.1002/mbo3.210
Ghequire MGK, Kemland L, Anoz-Carbonell E et al (2017a) A natural chimeric pseudomonas bacteriocin with novel pore-forming activity parasitizes the ferrichrome transporter. MBio 8:e01961–e01916. https://doi.org/10.1128/mBio.01961-16
Ghequire MGK, Kemland L, De Mot R (2017b) Novel immunity proteins associated with colicin M-like bacteriocins exhibit promiscuous protection in Pseudomonas. Front Microbiol 8:93. https://doi.org/10.3389/fmicb.2017.00093
Ghequire MGK, Swings T, Michiels J et al (2018) Hitting with a BAM: selective killing by lectin-like bacteriocins. MBio 9:e02138–e02117. https://doi.org/10.1128/mBio.02138-17
Ghoul M, West SA, Johansen HK et al (2015) Bacteriocin-mediated competition in cystic fibrosis lung infections. Proc Biol Sci 282:20150972. https://doi.org/10.1098/rspb.2015.0972
Gibson J, Sood A, Hogan DA (2009) Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl Environ Microbiol 75:504–513. https://doi.org/10.1128/AEM.01037-08
Gillies RR, Govan JR (1966) Ty** of Pseudomonas pyocyanea by pyocine production. J Pathol Bacteriol 91:339–345. https://doi.org/10.1002/path.1700910207
Govan JR (1974) Studies on the pyocins of Pseudomonas aeruginosa: production of contractile and flexuous pyocins in Pseudomonas aeruginosa. J Gen Microbiol 80:17–30. https://doi.org/10.1099/00221287-80-1-17
Haas H, Sacks T, Saltz N (1974) Protective effect of pyocin against lethal Pseudomonas aeruginosa infections in mice. J Infect Dis 129:470–472. https://doi.org/10.1093/infdis/129.4.470
Haba E, Pinazo A, Jauregui O et al (2003) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol Bioeng 81:316–322. https://doi.org/10.1002/bit.10474
Hachani A, Allsopp LP, Oduko Y, Filloux A (2014) The VgrG proteins are “à la carte” delivery systems for bacterial type VI effectors. J Biol Chem 289:17872–17884. https://doi.org/10.1074/jbc.M114.563429
Hamad MNF, Marrez DA, El-Sherbieny SMR (2020) Toxicity evaluation and antimicrobial activity of purified pyocyanin from Pseudomonas aeruginosa. Biointerface Res Appl Chem 10:6974–6990. https://doi.org/10.33263/BRIAC106.69746990
Han Y, Wang T, Chen G et al (2019) A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition. PLoS Pathog 15:e1008198. https://doi.org/10.1371/journal.ppat.1008198
Hassan HM, Fridovich I (1979) Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch Biochem Biophys 196:385–395. https://doi.org/10.1016/0003-9861(79)90289-3
Hassan HM, Fridovich I (1980) Mechanism of the antibiotic action pyocyanine. J Bacteriol 141:156–163. https://doi.org/10.1128/JB.141.1.156-163.1980
Heeb S, Fletcher MP, Chhabra SR et al (2011) Quinolones: from antibiotics to autoinducers. FEMS Microbiol Rev 35:247–274. https://doi.org/10.1111/j.1574-6976.2010.00247.x
Henderson IR, Navarro-Garcia F, Desvaux M et al (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68:692–744. https://doi.org/10.1128/MMBR.68.4.692-744.2004
Hernandez RE, Gallegos-Monterrosa R, Coulthurst SJ (2020) Type VI secretion system effector proteins: effective weapons for bacterial competitiveness. Cell Microbiol 22:e13241. https://doi.org/10.1111/cmi.13241
Hersch SJ, Manera K, Dong TG (2020a) Defending against the type six secretion system: beyond immunity genes. Cell Rep 33:108259. https://doi.org/10.1016/j.celrep.2020.108259
Hersch SJ, Watanabe N, Stietz MS et al (2020b) Envelope stress responses defend against type six secretion system attacks independently of immunity proteins. Nat Microbiol 5:706–714. https://doi.org/10.1038/s41564-020-0672-6
Higgins S, Heeb S, Rampioni G et al (2018) Differential regulation of the phenazine biosynthetic operons by quorum sensing in Pseudomonas aeruginosa PAO1-N. Front Cell Infect Microbiol 8:252. https://doi.org/10.3389/fcimb.2018.00252
Ho BT, Basler M, Mekalanos JJ (2013) Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer. Science 342:250–253. https://doi.org/10.1126/science.1243745
Ho BT, Fu Y, Dong TG, Mekalanos JJ (2017) Vibrio cholerae type 6 secretion system effector trafficking in target bacterial cells. Proc Natl Acad Sci U S A 114:9427–9432. https://doi.org/10.1073/pnas.1711219114
Hoffman LR, Déziel E, D’Argenio DA et al (2006) Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 103:19890–19895. https://doi.org/10.1073/pnas.0606756104
Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54:1212–1223. https://doi.org/10.1111/j.1365-2958.2004.04349.x
Hood RD, Singh P, Hsu F et al (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25–37. https://doi.org/10.1016/j.chom.2009.12.007
Hosono Honda N, Kimura S, Tateda K et al (2011) Roles of Pseudomonas aeruginosa autoinducers and their degradation products, tetramic acids, in bacterial survival and behavior in ecological niches. Microbes Environ 26:160–164. https://doi.org/10.1264/jsme2.me10198
Irie Y, O’Toole GA, Yuk MH (2005) Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol Lett 250:237–243. https://doi.org/10.1016/j.femsle.2005.07.012
Ishii S, Nishi Y, Egami F (1965) The fine structure of a pyocin. J Mol Biol 13:428-IN12. https://doi.org/10.1016/S0022-2836(65)80107-3
Ito S, Kageyama M, Egami F (1970) Isolation and characterization of pyocins from several strains of pseudomonas aeruginosa. J Gen Appl Microbiol 16:205–214. https://doi.org/10.2323/jgam.16.3_205
Ito S, Honda H, Tomita F, Suzuki T (1971) Rhamnolipids produced by Pseudomonas aeruginosa grown on n-paraffin (mixture of C 12 , C 13 and C 14 fractions). J Antibiot 24:855–859. https://doi.org/10.7164/antibiotics.24.855
Jacob F (1954) Induced biosynthesis and mode of action of a pyocine, antibiotic produced by Pseudomonas aeruginosa. Ann Inst Pasteur (Paris) 86:149–160. https://pubmed.ncbi.nlm.nih.gov/6771248/
Jamet A, Nassif X (2015) New players in the toxin field: polymorphic toxin systems in bacteria. MBio 6:e00285–e00215. https://doi.org/10.1128/mBio.00285-15
Jarvis FG, Johnson MJ (1949) A glyco-lipide produced by Pseudomonas Aeruginosa. J Am Chem Soc 71:4124–4126. https://doi.org/10.1021/ja01180a073
Jiang F, Waterfield NR, Yang J et al (2014) A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 15:600–610. https://doi.org/10.1016/j.chom.2014.04.010
Jiang F, Wang X, Wang B et al (2016) The Pseudomonas aeruginosa type VI secretion PGAP1-like effector induces host autophagy by activating endoplasmic reticulum stress. Cell Rep 16:1502–1509. https://doi.org/10.1016/j.celrep.2016.07.012
Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177:3998–4008. https://doi.org/10.1128/jb.177.14.3998-4008.1995
Kadurugamuwa JL, Beveridge TJ (1999) Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other gram-negative bacteria. Microbiology (Reading, Engl) 145(Pt 8):2051–2060. https://doi.org/10.1099/13500872-145-8-2051
Kadurugamuwa JL, Mayer A, Messner P et al (1998) S-layered Aneurinibacillus and Bacillus spp. are susceptible to the lytic action of Pseudomonas aeruginosa membrane vesicles. J Bacteriol 180:2306–2311. https://doi.org/10.1128/JB.180.9.2306-2311.1998
Kageyama M (1964) Studies of a pyocin. i. physical and chemical properties. J Biochem 55:49–53. https://doi.org/10.1093/oxfordjournals.jbchem.a127839
Kageyama M, Egami F (1962) On the purification and some properties of a pyocin, a bacteriocin produced by Pseudomonas aeruginosa. Life Sci 1:471–476. https://doi.org/10.1016/0024-3205(62)90055-3
Kaufmann GF, Sartorio R, Lee S-H et al (2005) Revisiting quorum sensing: discovery of additional chemical and biological functions for 3-oxo-N-acylhomoserine lactones. Proc Natl Acad Sci U S A 102:309–314. https://doi.org/10.1073/pnas.0408639102
Kaziro Y, Tanaka M (1965) Studies on the mode of action of pyocin. I. Inhibition of macromolecular synthesis in sensitive cells. J Biochem 57:689–695. https://www.jstage.jst.go.jp/article/biochemistry1922/57/5/57_5_689/_article
Kerr JR, Taylor GW, Rutman A et al (1999) Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J Clin Pathol 52:385–387. https://doi.org/10.1136/jcp.52.5.385
Kessler E, Safrin M, Olson JC, Ohman DE (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268:7503–7508. https://doi.org/10.1016/S0021-9258(18)53203-8
Kim YC, Tarr AW, Penfold CN (2014) Colicin import into E. coli cells: a model system for insights into the import mechanisms of bacteriocins. Biochim Biophys Acta 1843:1717–1731. https://doi.org/10.1016/j.bbamcr.2014.04.010
Kimura S, Tateda K, Ishii Y et al (2009) Pseudomonas aeruginosa Las quorum sensing autoinducer suppresses growth and biofilm production in Legionella species. Microbiology (Reading, Engl) 155:1934–1939. https://doi.org/10.1099/mic.0.026641-0
Köhler T, Donner V, van Delden C (2010) Lipopolysaccharide as shield and receptor for R-pyocin-mediated killing in Pseudomonas aeruginosa. J Bacteriol 192:1921–1928. https://doi.org/10.1128/JB.01459-09
Kumar RS, Ayyadurai N, Pandiaraja P et al (2005) Characterization of antifungal metabolite produced by a new strain Pseudomonas aeruginosa PUPa3 that exhibits broad-spectrum antifungal activity and biofertilizing traits. J Appl Microbiol 98:145–154. https://doi.org/10.1111/j.1365-2672.2004.02435.x
Kuroda K, Kageyama M (1979) Biochemical properties of a new flexuous bacteriocin, pyocin F1, produced by Pseudomonas aeruginosa. J Biochem 85:7–19. https://doi.org/10.1093/oxfordjournals.jbchem.a132332
Kuroda K, Kageyama M (1981) Comparative study of F-type pyocins of Pseudomonas aeruginosa. J Biochem 89:1721–1736. https://doi.org/10.1093/oxfordjournals.jbchem.a133372
LaCourse KD, Peterson SB, Kulasekara HD et al (2018) Conditional toxicity and synergy drive diversity among antibacterial effectors. Nat Microbiol 3:440–446. https://doi.org/10.1038/s41564-018-0113-y
Latifi A, Winson MK, Foglino M et al (1995) Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol 17:333–343. https://doi.org/10.1111/j.1365-2958.1995.mmi_17020333.x
Le N-H, Peters K, Espaillat A et al (2020) Peptidoglycan editing provides immunity to Acinetobacter baumannii during bacterial warfare. Sci Adv 6:eabb5614. https://doi.org/10.1126/sciadv.abb5614
Le NH, Pinedo V, Lopez J et al (2021) Killing of Gram-negative and Gram-positive bacteria by a bifunctional cell wall-targeting T6SS effector. Proc Natl Acad Sci U S A 118:e2106555118. https://doi.org/10.1073/pnas.2106555118
Lerat E, Moran NA (2004) The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 21:903–913. https://doi.org/10.1093/molbev/msh097
LeRoux M, Kirkpatrick RL, Montauti EI et al (2015) Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa. eLife 4:e05701. https://doi.org/10.7554/eLife.05701
Levin JC, Stein DC (1996) Cloning, complementation, and characterization of an rfaE homolog from Neisseria gonorrhoeae. J Bacteriol 178:4571–4575. https://doi.org/10.1128/jb.178.15.4571-4575.1996
Li Z, Clarke AJ, Beveridge TJ (1996) A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles. J Bacteriol 178:2479–2488. https://doi.org/10.1128/jb.178.9.2479-2488.1996
Li Z, Clarke AJ, Beveridge TJ (1998) Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J Bacteriol 180:5478–5483. https://doi.org/10.1128/JB.180.20.5478-5483.1998
Lin J, Zhang W, Cheng J et al (2017) A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nat Commun 8:14888. https://doi.org/10.1038/ncomms14888
Lin H-H, Filloux A, Lai E-M (2020) Role of recipient susceptibility factors during contact-dependent interbacterial competition. Front Microbiol 11:603652. https://doi.org/10.3389/fmicb.2020.603652
Ling H, Saeidi N, Rasouliha BH, Chang MW (2010) A predicted S-type pyocin shows a bactericidal activity against clinical Pseudomonas aeruginosa isolates through membrane damage. FEBS Lett 584:3354–3358. https://doi.org/10.1016/j.febslet.2010.06.021
Lizewski SE, Schurr JR, Jackson DW et al (2004) Identification of AlgR-regulated genes in Pseudomonas aeruginosa by use of microarray analysis. J Bacteriol 186:5672–5684. https://doi.org/10.1128/JB.186.17.5672-5684.2004
Lowery CA, Park J, Gloeckner C et al (2009) Defining the mode of action of tetramic acid antibacterials derived from Pseudomonas aeruginosa quorum sensing signals. J Am Chem Soc 131:14473–14479. https://doi.org/10.1021/ja9056079
Machan ZA, Taylor GW, Pitt TL et al (1992) 2-Heptyl-4-hydroxyquinoline N-oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa. J Antimicrob Chemother 30:615–623. https://doi.org/10.1093/jac/30.5.615
Magalhães L, Nitschke M (2013) Antimicrobial activity of rhamnolipids against Listeria monocytogenes and their synergistic interaction with nisin. Food Control 29:138–142. https://doi.org/10.1016/j.foodcont.2012.06.009
Maier RM, Soberón-Chávez G (2000) Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl Microbiol Biotechnol 54:625–633. https://doi.org/10.1007/s002530000443
Mandal PK, Ballerin G, Nolan LM et al (2021) Bacteriophage infection of Escherichia coli leads to the formation of membrane vesicles via both explosive cell lysis and membrane blebbing. Microbiology (Reading, Engl) 167:001021. https://doi.org/10.1099/mic.0.001021
Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422–425. https://doi.org/10.1038/nature03925
Matsui H, Sano Y, Ishihara H, Shinomiya T (1993) Regulation of pyocin genes in Pseudomonas aeruginosa by positive (prtN) and negative (prtR) regulatory genes. J Bacteriol 175:1257–1263. https://doi.org/10.1128/jb.175.5.1257-1263.1993
Mavrodi DV, Bonsall RF, Delaney SM et al (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–6465. https://doi.org/10.1128/JB.183.21.6454-6465.2001
McCaughey LC, Grinter R, Josts I et al (2014) Lectin-like bacteriocins from Pseudomonas spp. utilise D-rhamnose containing lipopolysaccharide as a cellular receptor. PLoS Pathog 10:e1003898. https://doi.org/10.1371/journal.ppat.1003898
Medina G, Juárez K, Valderrama B, Soberón-Chávez G (2003) Mechanism of Pseudomonas aeruginosa RhlR transcriptional regulation of the rhlAB promoter. J Bacteriol 185:5976–5983. https://doi.org/10.1128/jb.185.20.5976-5983.2003
Mei M, Thomas J, Diggle SP (2021) Heterogenous susceptibility to R-pyocins in populations of Pseudomonas aeruginosa sourced from cystic fibrosis lungs. MBio 12:e00458–e00421. https://doi.org/10.1128/mBio.00458-21
Melvin JA, Gaston JR, Phillips SN et al (2017) Pseudomonas aeruginosa contact-dependent growth inhibition plays dual role in host-pathogen interactions. mSphere 2:e00336-17. https://doi.org/10.1128/mSphere.00336-17
Mercy C, Ize B, Salcedo SP et al (2016) Functional characterization of pseudomonas contact dependent growth inhibition (CDI) systems. PLoS One 11:e0147435. https://doi.org/10.1371/journal.pone.0147435
Merrikin DJ, Terry CS (1972) Use of pyocin 78-C2 in the treatment of Pseudomonas aeruginosa infection in mice. Appl Microbiol 23:164–165. https://doi.org/10.1128/am.23.1.164-165.1972
Meuskens I, Saragliadis A, Leo JC, Linke D (2019) Type V secretion systems: an overview of passenger domain functions. Front Microbiol 10:1163. https://doi.org/10.3389/fmicb.2019.01163
Michel-Briand Y, Baysse C (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84:499–510. https://doi.org/10.1016/s0300-9084(02)01422-0
Mireles JR, Toguchi A, Harshey RM (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183:5848–5854. https://doi.org/10.1128/JB.183.20.5848-5854.2001
Monjarás Feria J, Valvano MA (2020) An overview of anti-eukaryotic T6SS effectors. Front Cell Infect Microbiol 10:584751. https://doi.org/10.3389/fcimb.2020.584751
Morales DK, Jacobs NJ, Rajamani S et al (2010) Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol Microbiol 78:1379–1392. https://doi.org/10.1111/j.1365-2958.2010.07414.x
Mougous JD, Cuff ME, Raunser S et al (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526–1530. https://doi.org/10.1126/science.1128393
Nakayama K, Takashima K, Ishihara H et al (2000) The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol 38:213–231. https://doi.org/10.1046/j.1365-2958.2000.02135.x
Nano FE, Zhang N, Cowley SC et al (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186:6430–6436. https://doi.org/10.1128/JB.186.19.6430-6436.2004
Nguyen AT, Jones JW, Cámara M et al (2016) Cystic fibrosis isolates of Pseudomonas aeruginosa retain iron-regulated antimicrobial activity against Staphylococcus aureus through the action of multiple alkylquinolones. Front Microbiol 7:1171. https://doi.org/10.3389/fmicb.2016.01171
Nolan LM, Cain AK, Clamens T et al (2021) Identification of Tse8 as a Type VI secretion system toxin from Pseudomonas aeruginosa that targets the bacterial transamidosome to inhibit protein synthesis in prey cells. Nat Microbiol 6:1199–1210. https://doi.org/10.1038/s41564-021-00950-8
Ochsner UA, Reiser J (1995) Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92:6424–6428. https://doi.org/10.1073/pnas.92.14.6424
Ohsumi M, Shinomiya T, Kageyama M (1980) Comparative study on R-type pyocins of Pseudomonas aeruginosa. J Biochem 87:1119–1125
Oluyombo O, Penfold CN, Diggle SP (2019) Competition in biofilms between cystic fibrosis isolates of Pseudomonas aeruginosa is shaped by R-pyocins. MBio 10:e01828–e01818. https://doi.org/10.1128/mBio.01828-18
Ong KS, Cheow YL, Lee SM (2017) The role of reactive oxygen species in the antimicrobial activity of pyochelin. J Advanc Res 8:393–398. https://doi.org/10.1016/j.jare.2017.05.007
Ortiz A, Teruel JA, Espuny MJ et al (2006) Effects of dirhamnolipid on the structural properties of phosphatidylcholine membranes. Int J Pharm 325:99–107. https://doi.org/10.1016/j.ijpharm.2006.06.028
Passador L, Cook JM, Gambello MJ et al (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127–1130. https://doi.org/10.1126/science.8493556
Pearson JP, Passador L, Iglewski BH, Greenberg EP (1995) A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92:1490–1494. https://doi.org/10.1073/pnas.92.5.1490
Perault AI, Chandler CE, Rasko DA et al (2020) Host adaptation predisposes Pseudomonas aeruginosa to type VI secretion system-mediated predation by the Burkholderia cepacia complex. Cell Host Microbe 28:534–547.e3. https://doi.org/10.1016/j.chom.2020.06.019
Pessi G, Haas D (2000) Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J Bacteriol 182:6940–6949. https://doi.org/10.1128/jb.182.24.6940-6949.2000
Pessi G, Williams F, Hindle Z et al (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183:6676–6683. https://doi.org/10.1128/JB.183.22.6676-6683.2001
Peters JE, Galloway DR (1990) Purification and characterization of an active fragment of the LasA protein from Pseudomonas aeruginosa: enhancement of elastase activity. J Bacteriol 172:2236–2240. https://doi.org/10.1128/jb.172.5.2236-2240.1990
Phillips NJ, John CM, Reinders LG et al (1990) Structural models for the cell surface lipooligosaccharides of Neisseria gonorrhoeae and Haemophilus influenzae. Biomed Environ Mass Spectrom 19:731–745. https://doi.org/10.1002/bms.1200191112
Pissaridou P, Allsopp LP, Wettstadt S et al (2018) The Pseudomonas aeruginosa T6SS-VgrG1b spike is topped by a PAAR protein eliciting DNA damage to bacterial competitors. Proc Natl Acad Sci U S A 115:12519–12524. https://doi.org/10.1073/pnas.1814181115
Pohlner J, Halter R, Beyreuther K, Meyer TF (1987) Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458–462. https://doi.org/10.1038/325458a0
Poole K, Neshat S, Krebes K, Heinrichs DE (1993) Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacteriol 175:4597–4604. https://doi.org/10.1128/jb.175.15.4597-4604.1993
Potvin E, Lehoux DE, Kukavica-Ibrulj I et al (2003) In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol 5:1294–1308. https://doi.org/10.1046/j.1462-2920.2003.00542.x
Pukatzki S, Ma AT, Sturtevant D et al (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103:1528–1533. https://doi.org/10.1073/pnas.0510322103
Qazi S, Middleton B, Muharram SH et al (2006) N-acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74:910–919. https://doi.org/10.1128/IAI.74.2.910-919.2006
Rahman PKSM, Pasirayi G, Auger V, Ali Z (2009) Development of a simple and low cost microbioreactor for high-throughput bioprocessing. Biotechnol Lett 31:209–214. https://doi.org/10.1007/s10529-008-9853-8
Raji El Feghali PA, Nawas T (2018) Pyocyanin: a powerful inhibitor of bacterial growth and biofilm formation. Madridge J Case Rep Stud 3:101–107. https://doi.org/10.18689/mjcrs-1000125
Rao PSS, Yamada Y, Tan YP, Leung KY (2004) Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol 53:573–586. https://doi.org/10.1111/j.1365-2958.2004.04123.x
Redero M, López-Causapé C, Aznar J et al (2018) Susceptibility to R-pyocins of Pseudomonas aeruginosa clinical isolates from cystic fibrosis patients. J Antimicrob Chemother 73:2770–2776. https://doi.org/10.1093/jac/dky261
Redero M, Aznar J, Prieto AI (2020) Antibacterial efficacy of R-type pyocins against Pseudomonas aeruginosa on biofilms and in a murine model of acute lung infection. J Antimicrob Chemother 75:2188–2196. https://doi.org/10.1093/jac/dkaa121
Reimmann C, Beyeler M, Latifi A et al (1997) The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol Microbiol 24:309–319. https://doi.org/10.1046/j.1365-2958.1997.3291701.x
Renelli M, Matias V, Lo RY, Beveridge TJ (2004) DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology (Reading, Engl) 150:2161–2169. https://doi.org/10.1099/mic.0.26841-0
Robb CS, Robb M, Nano FE, Boraston AB (2016) The Structure of the toxin and type six secretion system substrate Tse2 in complex with its immunity protein. Structure 24:277–284. https://doi.org/10.1016/j.str.2015.11.012
Robitaille S, Trus E, Ross BD (2021) Bacterial defense against the type VI secretion system. Trends Microbiol 29:187–190. https://doi.org/10.1016/j.tim.2020.09.001
Ruhe ZC, Wallace AB, Low DA, Hayes CS (2013) Receptor polymorphism restricts contact-dependent growth inhibition to members of the same species. MBio 4:e00480–e00413. https://doi.org/10.1128/mBio.00480-13
Ruhe ZC, Townsley L, Wallace AB et al (2015) CdiA promotes receptor-independent intercellular adhesion. Mol Microbiol 98:175–192. https://doi.org/10.1111/mmi.13114
Ruhe ZC, Nguyen JY, **ong J et al (2017) CdiA effectors use modular receptor-binding domains to recognize target bacteria. MBio 8:e00290–e00217. https://doi.org/10.1128/mBio.00290-17
Ruhe ZC, Subramanian P, Song K et al (2018) Programmed secretion arrest and receptor-triggered toxin export during antibacterial contact-dependent growth inhibition. Cell 175:921–933.e14. https://doi.org/10.1016/j.cell.2018.10.033
Russell AB, Hood RD, Bui NK et al (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343–347. https://doi.org/10.1038/nature10244
Russell AB, Singh P, Brittnacher M et al (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11:538–549. https://doi.org/10.1016/j.chom.2012.04.007
Russell AB, LeRoux M, Hathazi K et al (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496:508–512. https://doi.org/10.1038/nature12074
Saha S, Ojobor C, MacKinnon E et al (2021) F-type pyocins are diverse non-contractile phage tail-like weapons for killing Pseudomonas aeruginosa. BioRxiv. https://doi.org/10.1101/2021.02.16.431561
Sana TG, Baumann C, Merdes A et al (2015) Internalization of Pseudomonas aeruginosa strain PAO1 into epithelial cells is promoted by interaction of a T6SS effector with the microtubule network. MBio 6:e00712. https://doi.org/10.1128/mBio.00712-15
Sánchez M, Teruel JA, Espuny MJ et al (2006) Modulation of the physical properties of dielaidoylphosphatidylethanolamine membranes by a dirhamnolipid biosurfactant produced by Pseudomonas aeruginosa. Chem Phys Lipids 142:118–127. https://doi.org/10.1016/j.chemphyslip.2006.04.001
Sano Y, Kageyama M (1993) A novel transposon-like structure carries the genes for pyocin AP41, a Pseudomonas aeruginosa bacteriocin with a DNase domain homology to E2 group colicins. Mol Gen Genet 237:161–170. https://doi.org/10.1007/BF00282797
Sano Y, Matsui H, Kobayashi M, Kageyama M (1993) Molecular structures and functions of pyocins S1 and S2 in Pseudomonas aeruginosa. J Bacteriol 175:2907–2916. https://doi.org/10.1128/jb.175.10.2907-2916.1993
Saosoong K, Wongphathanakul W, Poasiri C, Ruangviriyachai C (2009) Isolation and analysis of antibacterial substance produced from P. aeruginosa TISTR 781. KKU Sci J 37:163–172
Schoental R (1941) The nature of the antibacterial agents present in Pseudomonas pyocyanea cultures. Br J Exp Pathol 22:137–147. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2065467/
Scholl D (2017) Phage tail-like bacteriocins. Annu Rev Virol 4:453–467. https://doi.org/10.1146/annurev-virology-101416-041632
Scholl D, Martin DW (2008) Antibacterial efficacy of R-type pyocins towards Pseudomonas aeruginosa in a murine peritonitis model. Antimicrob Agents Chemother 52:1647–1652. https://doi.org/10.1128/AAC.01479-07
Schooling SR, Charaf UK, Allison DG, Gilbert P (2004) A role for rhamnolipid in biofilm dispersion. Biofilms 1:91–99. https://doi.org/10.1017/S147905050400119X
Schooling SR, Hubley A, Beveridge TJ (2009) Interactions of DNA with biofilm-derived membrane vesicles. J Bacteriol 191:4097–4102. https://doi.org/10.1128/JB.00717-08
Seed PC, Passador L, Iglewski BH (1995) Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J Bacteriol 177:654–659. https://doi.org/10.1128/jb.177.3.654-659.1995
Sen S, Borah SN, Bora A, Deka S (2020) Rhamnolipid exhibits anti-biofilm activity against the dermatophytic fungi Trichophyton rubrum and Trichophyton mentagrophytes. Biotechnol Rep (Amst) 27:e00516. https://doi.org/10.1016/j.btre.2020.e00516
Seo Y, Galloway DR (1990) Purification of the pyocin S2 complex from Pseudomonas aeruginosa PAO1: analysis of DNase activity. Biochem Biophys Res Commun 172:455–461. https://doi.org/10.1016/0006-291x(90)90694-i
Sha R, Jiang L, Meng Q et al (2012) Producing cell-free culture broth of rhamnolipids as a cost-effective fungicide against plant pathogens. J Basic Microbiol 52:458–466. https://doi.org/10.1002/jobm.201100295
Shanmugaiah V, Mathivanan N, Varghese B (2010) Purification, crystal structure and antimicrobial activity of phenazine-1-carboxamide produced by a growth-promoting biocontrol bacterium, Pseudomonas aeruginosa MML2212. J Appl Microbiol 108:703–711. https://doi.org/10.1111/j.1365-2672.2009.04466.x
Shinomiya T (1972) Studies on biosynthesis and morphogenesis of R-type pyocins of Pseudomonas aeruginosa. 3. Subunits of pyocin R and their precipitability by anti-pyocin R serum. J Biochem 72:499–510. https://doi.org/10.1093/oxfordjournals.jbchem.a129929
Singh PK, Yadav VK, Kalia M et al (2017) Pseudomonas aeruginosa auto inducer3-oxo-C12-HSL exerts bacteriostatic effect and inhibits Staphylococcus epidermidis biofilm. Microb Pathog 110:612–619. https://doi.org/10.1016/j.micpath.2017.08.009
Smirnova IA, Hägerhäll C, Konstantinov AA, Hederstedt L (1995) HOQNO interaction with cytochrome b in succinate:menaquinone oxidoreductase from Bacillus subtilis. FEBS Lett 359:23–26. https://doi.org/10.1016/0014-5793(94)01442-4
Song L, Pan J, Yang Y et al (2021) Contact-independent killing mediated by a T6SS effector with intrinsic cell-entry properties. Nat Commun 12:423. https://doi.org/10.1038/s41467-020-20726-8
Sotirova AV, Spasova DI, Galabova DN et al (2008) Rhamnolipid-biosurfactant permeabilizing effects on gram-positive and gram-negative bacterial strains. Curr Microbiol 56:639–644. https://doi.org/10.1007/s00284-008-9139-3
Speare L, Cecere AG, Guckes KR et al (2018) Bacterial symbionts use a type VI secretion system to eliminate competitors in their natural host. Proc Natl Acad Sci U S A 115:E8528–E8537. https://doi.org/10.1073/pnas.1808302115
Stolle A-S, Meader BT, Toska J, Mekalanos JJ (2021) Endogenous membrane stress induces T6SS activity in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 118:e2018365118. https://doi.org/10.1073/pnas.2018365118
Su J-J, Zhou Q, Zhang H-Y et al (2010) Medium optimization for phenazine-1-carboxylic acid production by a gacA qscR double mutant of Pseudomonas sp. M18 using response surface methodology. Bioresour Technol 101:4089–4095. https://doi.org/10.1016/j.biortech.2009.12.143
Sudhakar T, Karpagam S (2011) Antifungal efficacy of pyocyanin produced from bioindicators of nosocomial hazards. In: International conference on green technology and environmental conservation (GTEC-2011). IEEE, pp 224–229. https://doi.org/10.1109/GTEC.2011.6167673
Takeya K, Minamishima Y, Amako K, Ohnishi Y (1967) A small rod-shaped pyocin. Virology 31:166–168. https://doi.org/10.1016/0042-6822(67)90021-9
Taylor NMI, Prokhorov NS, Guerrero-Ferreira RC et al (2016) Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 533:346–352. https://doi.org/10.1038/nature17971
Taylor NMI, van Raaij MJ, Leiman PG (2018) Contractile injection systems of bacteriophages and related systems. Mol Microbiol 108:6–15. https://doi.org/10.1111/mmi.13921
Ting S-Y, Martínez-García E, Huang S et al (2020) Targeted depletion of bacteria from mixed populations by programmable adhesion with antagonistic competitor cells. Cell Host Microbe 28:313–321.e6. https://doi.org/10.1016/j.chom.2020.05.006
Toder DS, Gambello MJ, Iglewski BH (1991) Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR. Mol Microbiol 5:2003–2010. https://doi.org/10.1111/j.1365-2958.1991.tb00822.x
Toska J, Ho BT, Mekalanos JJ (2018) Exopolysaccharide protects Vibrio cholerae from exogenous attacks by the type 6 secretion system. Proc Natl Acad Sci U S A 115:7997–8002. https://doi.org/10.1073/pnas.1808469115
Toyofuku M, Nomura N, Kuno E et al (2008) Influence of the Pseudomonas quinolone signal on denitrification in Pseudomonas aeruginosa. J Bacteriol 190:7947–7956. https://doi.org/10.1128/JB.00968-08
Toyofuku M, Nakajima-Kambe T, Uchiyama H, Nomura N (2010) The effect of a cell-to-cell communication molecule, Pseudomonas quinolone signal (PQS), produced by P. aeruginosa on other bacterial species. Microbes Environ 25:1–7. https://doi.org/10.1264/jsme2.me09156
Toyofuku M, Roschitzki B, Riedel K, Eberl L (2012) Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix. J Proteome Res 11:4906–4915. https://doi.org/10.1021/pr300395j
Tremblay J, Richardson A-P, Lépine F, Déziel E (2007) Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9:2622–2630. https://doi.org/10.1111/j.1462-2920.2007.01396.x
Trunk K, Peltier J, Liu Y-C et al (2018) The type VI secretion system deploys antifungal effectors against microbial competitors. Nat Microbiol 3:920–931. https://doi.org/10.1038/s41564-018-0191-x
Trunk K, Coulthurst SJ, Quinn J (2019) A new front in microbial warfare-delivery of antifungal effectors by the type VI secretion system. J Fungi (Basel) 5:50. https://doi.org/10.3390/jof5020050
Turnbull L, Toyofuku M, Hynen AL et al (2016) Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun 7:11220. https://doi.org/10.1038/ncomms11220
Turner JM, Messenger AJ (1986) Occurrence, biochemistry and physiology of phenazine pigment production. Adv Microb Physiol 27:211–275. https://doi.org/10.1016/S0065-2911(08)60306-9
Uratani Y, Hoshino T (1984) Pyocin R1 inhibits active transport in Pseudomonas aeruginosa and depolarizes membrane potential. J Bacteriol 157:632–636. https://doi.org/10.1128/jb.157.2.632-636.1984
Waksman SA, Woodruff HB (1942) Selective antibiotic action of various substances of microbial origin. J Bacteriol 44:373–384. https://doi.org/10.1128/jb.44.3.373-384.1942
Wang M, Schaefer AL, Dandekar AA, Greenberg EP (2015) Quorum sensing and policing of Pseudomonas aeruginosa social cheaters. Proc Natl Acad Sci U S A 112:2187–2191. https://doi.org/10.1073/pnas.1500704112
Wang J, Brodmann M, Basler M (2019) Assembly and subcellular localization of bacterial type VI secretion systems. Annu Rev Microbiol 73:621–638. https://doi.org/10.1146/annurev-micro-020518-115420
Wang T, Zhaoyu H, **ao D, Shi Y, Dang J, Lee M, Hesek D, Mobashery S, Min W, Liang H (2020) A type VI secretion system delivers a cell wall amidase to target bacterial competitors. Mol Microbiol 114(2):308–321. https://doi.org/10.1111/mmi.14513
Wang T, Du X, Ji L et al (2021) Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis. Cell Rep 35:108957. https://doi.org/10.1016/j.celrep.2021.108957
Webb JS, Nikolakakis KC, Willett JLE et al (2013) Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition. PLoS One 8:e57609. https://doi.org/10.1371/journal.pone.0057609
Wettstadt S, Wood TE, Fecht S, Filloux A (2019) Delivery of the Pseudomonas aeruginosa phospholipase effectors PldA and PldB in a VgrG- and H2-T6SS-dependent manner. Front Microbiol 10:1718. https://doi.org/10.3389/fmicb.2019.01718
Whitney JC, Beck CM, Goo YA et al (2014) Genetically distinct pathways guide effector export through the type VI secretion system. Mol Microbiol 92:529–542. https://doi.org/10.1111/mmi.12571
Whitney JC, Quentin D, Sawai S et al (2015) An interbacterial NAD(P)(+) glycohydrolase toxin requires elongation factor Tu for delivery to target cells. Cell 163:607–619. https://doi.org/10.1016/j.cell.2015.09.027
Wilderman PJ, Vasil AI, Johnson Z, Vasil ML (2001) Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol Microbiol 39:291–303. https://doi.org/10.1046/j.1365-2958.2001.02282.x
Willett JLE, Gucinski GC, Fatherree JP et al (2015) Contact-dependent growth inhibition toxins exploit multiple independent cell-entry pathways. Proc Natl Acad Sci U S A 112:11341–11346. https://doi.org/10.1073/pnas.1512124112
Williams HD, Zlosnik JEA, Ryall B (2006) Oxygen, cyanide and energy generation in the cystic fibrosis pathogen Pseudomonas aeruginosa. Elsevier, pp 1–71. https://doi.org/10.1016/S0065-2911(06)52001-6
Winson MK, Camara M, Latifi A et al (1995) Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92:9427–9431. https://doi.org/10.1073/pnas.92.20.9427
Wood TL, Gong T, Zhu L et al (2018) Rhamnolipids from Pseudomonas aeruginosa disperse the biofilms of sulfate-reducing bacteria. npj Biofilms Microbiomes 4:22. https://doi.org/10.1038/s41522-018-0066-1
Wood TE, Howard SA, Förster A et al (2019a) The Pseudomonas aeruginosa T6SS delivers a periplasmic toxin that disrupts bacterial cell morphology. Cell Rep 29:187–201.e7. https://doi.org/10.1016/j.celrep.2019.08.094
Wood TE, Howard SA, Wettstadt S, Filloux A (2019b) PAAR proteins act as the “sorting hat” of the type VI secretion system. Microbiology (Reading, Engl) 165:1203–1218. https://doi.org/10.1099/mic.0.000842
Wratten SJ, Wolfe MS, Andersen RJ, Faulkner DJ (1977) Antibiotic metabolites from a marine pseudomonad. Antimicrob Agents Chemother 11:411–414. https://doi.org/10.1128/AAC.11.3.411
Yan H, Asfahl KL, Li N et al (2019) Conditional quorum-sensing induction of a cyanide-insensitive terminal oxidase stabilizes cooperating populations of Pseudomonas aeruginosa. Nat Commun 10:4999. https://doi.org/10.1038/s41467-019-13013-8
Young G (1947) Pigment production and antibiotic activity in cultures of Pseudomonas aeruginosa. J Bacteriol 54:109–117. https://doi.org/10.1128/jb.54.2.109-117.1947
Zhang D, de Souza RF, Anantharaman V et al (2012) Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 7:18. https://doi.org/10.1186/1745-6150-7-18
Zhang L, Tian X, Kuang S et al (2017) Antagonistic activity and mode of action of phenazine-1-carboxylic acid, produced by marine bacterium Pseudomonas aeruginosa PA31x, against Vibrio anguillarum in vitro and in a zebrafish in vivo model. Front Microbiol 8:289. https://doi.org/10.3389/fmicb.2017.00289
Zhao X, Chen Z, Yu L et al (2017) Investigating the antifungal activity and mechanism of a microbial pesticide Shenqinmycin against Phoma sp. Pestic Biochem Physiol 147:46–50. https://doi.org/10.1016/j.pestbp.2017.08.014
Acknowledgments
We apologise to authors whose work was not cited due to space restrictions. During the preparation of this chapter, LMN was supported by an Imperial College Research Fellowship and LPA was supported by the National Heart and Lung Institute at Imperial College London. Both LMN and LPA are in an environment that received funds from the Cystic Fibrosis Trust to establish the Strategic Research Centre: Personalized approach to P. aeruginosa. Figures 8.1 and 8.3 were created with https://BioRender.com.
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Nolan, L.M., Allsopp, L.P. (2022). Antimicrobial Weapons of Pseudomonas aeruginosa. In: Filloux, A., Ramos, JL. (eds) Pseudomonas aeruginosa. Advances in Experimental Medicine and Biology, vol 1386. Springer, Cham. https://doi.org/10.1007/978-3-031-08491-1_8
Download citation
DOI: https://doi.org/10.1007/978-3-031-08491-1_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-08490-4
Online ISBN: 978-3-031-08491-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)