Bacterial antagonism in host-associated microbial communities

Science

Volumn 361, Issue 6408, 2018, Pages

  García Bayona, Leonor ^a   Comstock, Laurie E ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; POLYMORPHIC TOXIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; BACTERIAL TOXIN;

ANTAGONISM; BACTERIUM; CELL; ECOLOGICAL IMPACT; LONG-TERM CHANGE; MICROBIAL COMMUNITY; PEPTIDE; PROTEIN;

ANTIBIOSIS; ANTIBIOTIC RESISTANCE; BIOLOGICAL THERAPY; CELL KILLING; CYTOLYSIS; EXPERIMENTAL MODEL; HEALTH PROMOTION; HOST PATHOGEN INTERACTION; HUMAN; IN VIVO STUDY; MATHEMATICAL MODEL; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; ORGANISM COMMUNITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SPECIES INVASION; TARGET CELL; TRANSGENIC MICROORGANISM; TREATMENT FAILURE; TYPE IV SECRETION SYSTEM; TYPE V SECRETION SYSTEM; TYPE VI SECRETION SYSTEM; TYPE VII SECRETION SYSTEM; ANIMAL; BACTERIAL INFECTION; BACTERIAL SECRETION SYSTEM; BACTEROIDES; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; MICROFLORA; ORGANISMAL INTERACTION; PHYSIOLOGY; SYMBIOSIS;

BACTERIA (MICROORGANISMS);

ANIMALS; BACTERIAL INFECTIONS; BACTERIAL SECRETION SYSTEMS; BACTERIAL TOXINS; BACTEROIDES; GASTROINTESTINAL MICROBIOME; HUMANS; MICROBIAL INTERACTIONS; MICROBIOTA; SYMBIOSIS;

EID: 85054038525     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aat2456     Document Type: Review

References (136)

1. M. E. Hibbing, C. Fuqua, M. R. Parsek, S. B. Peterson, Bacterial competition: Surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010). doi: 10.1038/nrmicro2259; pmid: 19946288
2. M. Ghoul, S. Mitri, The ecology and evolution of microbial competition. Trends Microbiol. 24, 833–845 (2016). doi: 10.1016/j.tim.2016.06.011; pmid: 27546832
3. A. J. Bäumler, V. Sperandio, Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535, 85–93 (2016). doi: 10.1038/nature18849; pmid: 27383983
4. J. J. Faith et al., The long-term stability of the human gut microbiota. Science 341, 1237439 (2013). doi: 10.1126/science.1237439; pmid: 23828941
5. A. Moya, M. Ferrer, Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 24, 402–413 (2016). doi: 10.1016/j.tim.2016.02.002; pmid: 26996765
6. A. E. F. Little, C. J. Robinson, S. B. Peterson, K. F. Raffa, J. Handelsman, Rules of engagement: Interspecies interactions that regulate microbial communities. Annu. Rev. Microbiol. 62, 375–401 (2008). doi: 10.1146/annurev.micro.030608.101423; pmid: 18544040
7. C. G. Buffie et al., Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517, 205–208 (2015). doi: 10.1038/nature13828; pmid: 25337874
8. B. S. Weber, P. M. Ly, J. N. Irwin, S. Pukatzki, M. F. Feldman, A multidrug resistance plasmid contains the molecular switch for type VI secretion in Acinetobacter baumannii. Proc. Natl. Acad. Sci. U.S.A. 112, 9442–9447 (2015). doi: 10.1073/pnas.1502966112; pmid: 26170289
9. E. L. Miller et al., Eavesdropping and crosstalk between secreted quorum sensing peptide signals that regulate bacteriocin production in Streptococcus pneumoniae. ISME J (2018). doi: 10.1038/s41396-018-0178-x; pmid: 29899510
10. R. S. Mehta et al., Stability of the human faecal microbiome in a cohort of adult men. Nat. Microbiol. 3, 347–355 (2018). doi: 10.1038/s41564-017-0096-0; pmid: 29335554
11. T. N. Jayasinghe et al., Long-term stability in the gut microbiome over 46 years in the life of Billy Apple. Hum. Microbiome J. 5–6, 7–10 (2017). doi: 10.1016/j.humic.2017.09.001
12. K. Z. Coyte, J. Schluter, K. R. Foster, The ecology of the microbiome: Networks, competition, and stability. Science 350, 663–666 (2015). doi: 10.1126/science.aad2602; pmid: 26542567
13. M. I. Abrudan, S. Brown, D. E. Rozen, Killing as means of promoting biodiversity. Biochem. Soc. Trans. 40, 1512–1516 (2012). doi: 10.1042/BST20120196; pmid: 23176508
14. P. Szabó, T. Czárán, G. Szabó, Competing associations in bacterial warfare with two toxins. J. Theor. Biol. 248, 736–744 (2007). doi: 10.1016/j.jtbi.2007.06.022; pmid: 17686495
15. B. Kerr, M. A. Riley, M. W. Feldman, B. J. M. Bohannan, Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418, 171–174 (2002). doi: 10.1038/nature00823; pmid: 12110887
16. B. C. Kirkup, M. A. Riley, Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 428, 412–414 (2004). doi: 10.1038/nature02429; pmid: 15042087
17. M. Wong et al., Microbial herd protection mediated by antagonistic interaction in polymicrobial communities. Appl. Environ. Microbiol. 82, 6881–6888 (2016). doi: 10.1128/AEM.02210-16; pmid: 27637882
18. O. Rendueles, M. Amherd, G. J. Velicer, Positively frequency-dependent interference competition maintains diversity and pervades a natural population of cooperative microbes. Curr. Biol. 25, 1673–1681 (2015). doi: 10.1016/j.cub.2015.04.057; pmid: 26051889
19. P. D. Cotter, R. P. Ross, C. Hill, Bacteriocins—A viable alternative to antibiotics? Nat. Rev. Microbiol. 11, 95–105 (2013). doi: 10.1038/nrmicro2937; pmid: 23268227
20. M. A. Riley, in Encyclopedia of Microbiology (Elsevier, 2009), pp. 32–44.
21. E. Riboulet-Bisson et al., Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota. PLOS ONE 7, e31113 (2012). doi: 10.1371/journal.pone.0031113; pmid: 22363561
22. M. Chatzidaki-Livanis, M. J. Coyne, L. E. Comstock, An antimicrobial protein of the gut symbiont Bacteroides fragilis with a MACPF domain of host immune proteins. Mol. Microbiol. 94, 1361–1374 (2014). doi: 10.1111/mmi.12839; pmid: 25339613
23. K. G. Roelofs, M. J. Coyne, R. R. Gentyala, M. Chatzidaki-Livanis, L. E. Comstock, Bacteroidales secreted antimicrobial proteins target surface molecules necessary for gut colonization and mediate competition in vivo. MBio 7, e01055-e16 (2016). doi: 10.1128/mBio.01055-16; pmid: 27555309
24. A. B. Russell et al., A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 16, 227–236 (2014). doi: 10.1016/j.chom.2014.07.007; pmid: 25070807
25. M. J. Coyne, N. L. Zitomersky, A. M. McGuire, A. M. Earl, L. E. Comstock, Evidence of extensive DNA transfer between bacteroidales species within the human gut. MBio 5, e01305–e01314 (2014). doi: 10.1128/mBio.01305-14; pmid: 24939888
26. M. J. Coyne, K. G. Roelofs, L. E. Comstock, Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics 17, 58 (2016). doi: 10.1186/s12864-016-2377-z; pmid: 26768901
27. M. Chatzidaki-Livanis, N. Geva-Zatorsky, L. E. Comstock, Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc. Natl. Acad. Sci. U.S.A. 113, 3627–3632 (2016). doi: 10.1073/pnas.1522510113; pmid: 26951680
28. A. L. Hecht et al., Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep. 17, 1281–1291 (2016). doi: 10.15252/embr.201642282; pmid: 27432285
29. A. G. Wexler et al., Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc. Natl. Acad. Sci. U.S.A. 113, 3639–3644 (2016). doi: 10.1073/pnas.1525637113; pmid: 26957597
30. N. A. Pudlo et al., Symbiotic human gut bacteria with variable metabolic priorities for host mucosal glycans. MBio 6, e01282–e15 (2015). doi: 10.1128/mBio.01282-15; pmid: 26556271
31. S. M. Lee et al., Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426–429 (2013). doi: 10.1038/nature12447; pmid: 23955152
32. J. C. Whitney et al., A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. eLife 6, e26938 (2017). doi: 10.7554/eLife.26938; pmid: 28696203
33. J. Chu et al., Discovery of MRSA active antibiotics using primary sequence from the human microbiome. Nat. Chem. Biol. 12, 1004–1006 (2016). doi: 10.1038/nchembio.2207; pmid: 27748750
34. M. S. Donia et al., A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell 158, 1402–1414 (2014). doi: 10.1016/j.cell.2014.08.032; pmid: 25215495
35. S. Kommineni et al., Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526, 719–722 (2015). doi: 10.1038/nature15524; pmid: 26479034
36. K. J. Rangan, H. C. Hang, Biochemical mechanisms of pathogen restriction by intestinal bacteria. Trends Biochem. Sci. 42, 887–898 (2017). doi: 10.1016/j.tibs.2017.08.005; pmid: 28927699
37. M. Sassone-Corsi et al., Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature 540, 280–283 (2016). doi: 10.1038/nature20557; pmid: 27798599
38. S. C. Corr et al., Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc. Natl. Acad. Sci. U.S.A. 104, 7617–7621 (2007). doi: 10.1073/pnas.0700440104; pmid: 17456596
39. D. Janek, A. Zipperer, A. Kulik, B. Krismer, A. Peschel, High frequency and diversity of antimicrobial activities produced by nasal Staphylococcus strains against bacterial competitors. PLOS Pathog. 12, e1005812 (2016). doi: 10.1371/journal.ppat.1005812; pmid: 27490492
40. A. Zipperer et al., Human commensals producing a novel antibiotic impair pathogen colonization. Nature 535, 511–516 (2016). doi: 10.1038/nature18634; pmid: 27466123
41. Y. Turovskiy, R. D. Ludescher, A. A. Aroutcheva, S. Faro, M. L. Chikindas, Lactocin 160, a bacteriocin produced by vaginal Lactobacillus rhamnosus, targets cytoplasmic membranes of the vaginal pathogen, Gardnerella vaginalis. Probiotics Antimicrob. Proteins 1, 67–74 (2009). doi: 10.1007/s12602-008-9003-6; pmid: 20445810
42. A. Maldonado-Barragán, B. Caballero-Guerrero, V. Martín, J. L. Ruiz-Barba, J. M. Rodríguez, Purification and genetic characterization of gassericin E, a novel co-culture inducible bacteriocin from Lactobacillus gasseri EV1461 isolated from the vagina of a healthy woman. BMC Microbiol. 16, 37 (2016). doi: 10.1186/s12866-016-0663-1; pmid: 26969428
43. P. Bernal, L. P. Allsopp, A. Filloux, M. A. Llamas, The Pseudomonas putida T6SS is a plant warden against phytopathogens. ISME J. 11, 972–987 (2017). doi: 10.1038/ismej.2016.169; pmid: 28045455
44. J. D. Palmer et al., Engineered probiotic for the inhibition of Salmonella via tetrathionate-induced production of microcin H47. ACS Infect. Dis. 4, 39–45 (2018). doi: 10.1021/acsinfecdis.7b00114; pmid: 28918634
45. S. Gupta, E. E. Bram, R. Weiss, Genetically programmable pathogen sense and destroy. ACS Synth. Biol. 2, 715–723 (2013). doi: 10.1021/sb4000417; pmid: 23763381
46. J. Borrero, Y. Chen, G. M. Dunny, Y. N. Kaznessis, Modified lactic acid bacteria detect and inhibit multiresistant enterococci. ACS Synth. Biol. 4, 299–306 (2015). doi: 10.1021/sb500090b; pmid: 24896372
47. S. E. Winter et al., Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339, 708–711 (2013). doi: 10.1126/science.1232467; pmid: 23393266
48. S. E. Winter et al., Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426–429 (2010). doi: 10.1038/nature09415; pmid: 20864996
49. M. X. Byndloss, A. J. Bäumler, The germ-organ theory of non-communicable diseases. Nat. Rev. Microbiol. 16, 103–110 (2018). doi: 10.1038/nrmicro.2017.158; pmid: 29307890
50. L. P. Nedialkova et al., Inflammation fuels colicin Ib-dependent competition of Salmonella serovar Typhimurium and E. coli in enterobacterial blooms. PLOS Pathog. 10, e1003844 (2014). doi: 10.1371/journal.ppat.1003844; pmid: 24391500
51. T. G. Sana et al., Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc. Natl. Acad. Sci. U.S.A. 113, E5044–E5051 (2016). doi: 10.1073/pnas.1608858113; pmid: 27503894
52. D. Pezoa et al., Only one of the two type VI secretion systems encoded in the Salmonella enterica serotype Dublin genome is involved in colonization of the avian and murine hosts. Vet. Res. 45, 2 (2014). doi: 10.1186/1297-9716-45-2; pmid: 24405577
53. M. C. Anderson, P. Vonaesch, A. Saffarian, B. S. Marteyn, P. J. Sansonetti, Shigella sonnei encodes a functional T6SS used for interbacterial competition and niche occupancy. Cell Host Microbe 21, 769–776.e3 (2017). doi: 10.1016/j.chom.2017.05.004; pmid: 28618272
54. W. Zhao, F. Caro, W. Robins, J. J. Mekalanos, Antagonism toward the intestinal microbiota and its effect on Vibrio cholerae virulence. Science 359, 210–213 (2018). doi: 10.1126/science.aap8775; pmid: 29326272
55. J. J. Quereda et al., Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. Proc. Natl. Acad. Sci. U.S.A. 113, 5706–5711 (2016). doi: 10.1073/pnas.1523899113; pmid: 27140611
56. L.-S. Ma, A. Hachani, J.-S. Lin, A. Filloux, E.-M. Lai, Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16, 94–104 (2014). doi: 10.1016/j.chom.2014.06.002; pmid: 24981331
57. D. P. Souza et al., Bacterial killing via a type IV secretion system. Nat. Commun. 6, 6453 (2015). doi: 10.1038/ncomms7453; pmid: 25743609
58. A. Darsonval et al., Adhesion and fitness in the bean phyllosphere and transmission to seed of Xanthomonas fuscans subsp. fuscans. Mol. Plant Microbe Interact. 22, 747–757 (2009). doi: 10.1094/MPMI-22-6-0747; pmid: 19445599
59. C. M. Rojas, J. H. Ham, W.-L. Deng, J. J. Doyle, A. Collmer, HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc. Natl. Acad. Sci. U.S.A. 99, 13142–13147 (2002). doi: 10.1073/pnas.202358699; pmid: 12271135
60. E. Shanker, M. J. Federle, Quorum sensing regulation of competence and bacteriocins in Streptococcus pneumoniae and mutans. Genes (Basel) 8, 15 (2017). doi: 10.3390/genes8010015; pmid: 28067778
61. W.-Y. Wholey, T. J. Kochan, D. N. Storck, S. Dawid, Coordinated bacteriocin expression and competence in Streptococcus pneumoniae contributes to genetic adaptation through neighbor predation. PLOS Pathog. 12, e1005413 (2016). doi: 10.1371/journal.ppat.1005413; pmid: 26840124
62. C. Y. Wang, S. Dawid, Mobilization of Bacteriocins during competence in Streptococci. Trends Microbiol. 26, 389–391 (2018). doi: 10.1016/j.tim.2018.03.002; pmid: 29588109
63. S. Borgeaud, L. C. Metzger, T. Scrignari, M. Blokesch, The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 347, 63–67 (2015). doi: 10.1126/science.1260064; pmid: 25554784
64. J. Thomas, S. S. Watve, W. C. Ratcliff, B. K. Hammer, Horizontal gene transfer of functional type VI killing genes by natural transformation. MBio 8, e00654-17 (2017). doi: 10.1128/mBio.00654-17; pmid: 28743812
65. P. C. Kirchberger, D. Unterweger, D. Provenzano, S. Pukatzki, Y. Boucher, Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae. Sci. Rep. 7, 45133 (2017). doi: 10.1038/srep45133; pmid: 28327641
66. D. Wall, Kin recognition in bacteria. Annu. Rev. Microbiol. 70, 143–160 (2016). doi: 10.1146/annurev-micro-102215-095325; pmid: 27359217
67. J. B. Bruce, G. A. Cooper, H. Chabas, S. A. West, A. S. Griffin, Cheating and resistance to cheating in natural populations of the bacterium Pseudomonas fluorescens. Evolution 71, 2484–2495 (2017). doi: 10.1111/evo.13328; pmid: 28833073
68. C. Majerczyk, E. Schneider, E. P. Greenberg, Quorum sensing control of Type VI secretion factors restricts the proliferation of quorum-sensing mutants. eLife 5, e14712 (2016). doi: 10.7554/eLife.14712; pmid: 27183270
69. C. N. Vassallo et al., Infectious polymorphic toxins delivered by outer membrane exchange discriminate kin in myxobacteria. eLife 6, e29397 (2017). doi: 10.7554/eLife.29397; pmid: 28820387
70. N. A. Lyons, B. Kraigher, P. Stefanic, I. Mandic-Mulec, R. Kolter, A combinatorial kin discrimination system in Bacillus subtilis. Curr. Biol. 26, 733–742 (2016). doi: 10.1016/j.cub.2016.01.032; pmid: 26923784
71. L. McNally et al., Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat. Commun. 8, 14371 (2017). doi: 10.1038/ncomms14371; pmid: 28165005
72. C. J. Alteri et al., Multicellular bacteria deploy the type VI secretion system to preemptively strike neighboring cells. PLOS Pathog. 9, e1003608 (2013).
73. E. C. Garcia, Contact-dependent interbacterial toxins deliver a message. Curr. Opin. Microbiol. 42, 40–46 (2018). doi: 10.1016/j.mib.2017.09.011; pmid: 29078204
74. E. S. Danka, E. C. Garcia, P. A. Cotter, Are CDI systems multicolored, facultative, helping greenbeards? Trends Microbiol. 25, 391–401 (2017). doi: 10.1016/j.tim.2017.02.008; pmid: 28285908
75. D. B. Borenstein, P. Ringel, M. Basler, N. S. Wingreen, Established microbial colonies can survive Type VI secretion assault. PLOS Comput. Biol. 11, e1004520 (2015). doi: 10.1371/journal.pcbi.1004520; pmid: 26485125
76. P. L. Conlin, J. R. Chandler, B. Kerr, Games of life and death: Antibiotic resistance and production through the lens of evolutionary game theory. Curr. Opin. Microbiol. 21, 35–44 (2014). doi: 10.1016/j.mib.2014.09.004; pmid: 25271120
77. M. Lazzaro, M. F. Feldman, E. García Véscovi, A transcriptional regulatory mechanism finely tunes the firing of Type VI secretion system in response to bacterial enemies. MBio 8, e00559-17 (2017). doi: 10.1128/mBio.00559-17; pmid: 28830939
78. M. Basler, M. Pilhofer, G. P. Henderson, G. J. Jensen, J. J. Mekalanos, Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483, 182–186 (2012). doi: 10.1038/nature10846; pmid: 22367545
79. C. M. Guinane et al., Impact of environmental factors on bacteriocin promoter activity in gut-derived Lactobacillus salivarius. Appl. Environ. Microbiol. 81, 7851–7859 (2015). doi: 10.1128/AEM.02339-15; pmid: 26341205
80. V. Bachmann et al., Bile salts modulate the mucin-activated type VI secretion system of pandemic Vibrio cholerae. PLOS Negl. Trop. Dis. 9, e0004031 (2015). doi: 10.1371/journal.pntd.0004031; pmid: 26317760
81. A. K. Korgaonkar, M. Whiteley, Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan. J. Bacteriol. 193, 909–917 (2011). doi: 10.1128/JB.01175-10; pmid: 21169497
82. A. Venkataraman, M. A. Rosenbaum, J. J. Werner, S. C. Winans, L. T. Angenent, Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa. ISME J. 8, 1210–1220 (2014). doi: 10.1038/ismej.2013.232; pmid: 24401856
83. D. M. Cornforth, K. R. Foster, Competition sensing: The social side of bacterial stress responses. Nat. Rev. Microbiol. 11, 285–293 (2013). doi: 10.1038/nrmicro2977; pmid: 23456045
84. M. Basler, B. T. Ho, J. J. Mekalanos, Tit-for-tat: Type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152, 884–894 (2013). doi: 10.1016/j.cell.2013.01.042; pmid: 23415234
85. M. LeRoux et al., Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc. Natl. Acad. Sci. U.S.A. 109, 19804–19809 (2012). doi: 10.1073/pnas.1213963109; pmid: 23150540
86. S. Rebuffat, Microcins in action: Amazing defence strategies of Enterobacteria. Biochem. Soc. Trans. 40, 1456–1462 (2012). doi: 10.1042/BST20120183; pmid: 23176498
87. G. Vassiliadis, D. Destoumieux-Garzón, C. Lombard, S. Rebuffat, J. Peduzzi, Isolation and characterization of two members of the siderophore-microcin family, microcins M and H47. Antimicrob. Agents Chemother. 54, 288–297 (2010). doi: 10.1128/AAC.00744-09; pmid: 19884380
88. X. Thomas et al., Siderophore peptide, a new type of post-translationally modified antibacterial peptide with potent activity. J. Biol. Chem. 279, 28233–28242 (2004). doi: 10.1074/jbc.M400228200; pmid: 15102848
89. M. LeRoux, S. B. Peterson, J. D. Mougous, Bacterial danger sensing. J. Mol. Biol. 427, 3744–3753 (2015). doi: 10.1016/j.jmb.2015.09.018; pmid: 26434507
90. S. Westhoff, G. P. van Wezel, D. E. Rozen, Distance-dependent danger responses in bacteria. Curr. Opin. Microbiol. 36, 95–101 (2017). doi: 10.1016/j.mib.2017.02.002; pmid: 28258981
91. M. LeRoux et al., Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa. eLife 4, e05701 (2015). doi: 10.7554/eLife.05701; pmid: 25643398
92. J. R. Chandler, S. Heilmann, J. E. Mittler, E. P. Greenberg, Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model. ISME J. 6, 2219–2228 (2012). doi: 10.1038/ismej.2012.69; pmid: 22763647
93. R. P. Ryan et al., Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol. Microbiol. 68, 75–86 (2008). doi: 10.1111/j.1365-2958.2008.06132.x; pmid: 18312265
94. R. Levy, E. Borenstein, Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules. Proc. Natl. Acad. Sci. U.S.A. 110, 12804–12809 (2013). doi: 10.1073/pnas.1300926110; pmid: 23858463
95. P. D. Ringel, D. Hu, M. Basler, The role of type VI secretion system effectors in target cell lysis and subsequent horizontal gene transfer. Cell Reports 21, 3927–3940 (2017). doi: 10.1016/j.celrep.2017.12.020; pmid: 29281838
96. H. J. Haiser et al., Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 341, 295–298 (2013). doi: 10.1126/science.1235872; pmid: 23869020
97. V. Gopalakrishnan et al., Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359, 97–103 (2018). doi: 10.1126/science.aan4236; pmid: 29097493
98. B. Routy et al., Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359, 91–97 (2018). doi: 10.1126/science.aan3706; pmid: 29097494
99. V. Matson et al., The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359, 104–108 (2018). doi: 10.1126/science.aao3290; pmid: 29302014
100. E. Breukink, B. de Kruijff, The lantibiotic nisin, a special case or not? Biochim. Biophys. Acta 1462, 223–234 (1999). doi: 10.1016/S0005-2736(99)00208-4; pmid: 10590310
101. N. Fimland, P. Rogne, G. Fimland, J. Nissen-Meyer, P. E. Kristiansen, Three-dimensional structure of the two peptides that constitute the two-peptide bacteriocin plantaricin EF. Biochim. Biophys. Acta 1784, 1711–1719 (2008). doi: 10.1016/j.bbapap.2008.05.003 pmid: 18555030
102. N. V. Dudkina et al., Structure of the poly-C9 component of the complement membrane attack complex. Nat. Commun. 7, 10588 (2016). doi: 10.1038/ncomms10588; pmid: 26841934
103. S. Soelaiman, K. Jakes, N. Wu, C. Li, M. Shoham, Crystal structure of colicin E3: Implications for cell entry and ribosome inactivation. Mol. Cell 8, 1053–1062 (2001). doi: 10.1016/S1097-2765(01)00396-3; pmid: 11741540
104. Z. C. Ruhe et al., CdiA effectors use modular receptor-binding domains to recognize target bacteria. MBio 8, e00290-17 (2017). doi: 10.1128/mBio.00290-17; pmid: 28351921
105. A. Besse, J. Peduzzi, S. Rebuffat, A. Carré-Mlouka, Antimicrobial peptides and proteins in the face of extremes: Lessons from archaeocins. Biochimie 118, 344–355 (2015). doi: 10.1016/j.biochi.2015.06.004; pmid: 26092421
106. M. A. Riley, in Prokaryotic Antimicrobial Peptides, D. Drider, S. Rebuffat, Eds. (Springer New York, 2011), pp. 13–26.
107. S. Rebuffat, in Prokaryotic Antimicrobial Peptides, D. Drider, S. Rebuffat, Eds. (Springer New York, 2011), pp. 55–72.
108. I. F. Nes, in Prokaryotic Antimicrobial Peptides, D. Drider, S. Rebuffat, Eds. (Springer New York, 2011), pp. 3–12.
109. D. M. Gordon, E. Oliver, J. Littlefield-Wyer, in Bacteriocins, M. A. Riley, M. A. Chavan, Eds. (Springer Berlin Heidelberg, 2007), pp. 5–18.
110. N. C. K. Heng, P. A. Wescombe, J. P. Burton, R. W. Jack, J. R. Tagg, in Bacteriocins, M. A. Riley, M. A. Chavan, Eds. (Springer Berlin Heidelberg, 2007), pp. 45–92.
111. M. C. Rea, R. P. Ross, P. D. Cotter, C. Hill, in Prokaryotic Antimicrobial Peptides, D. Drider, S. Rebuffat, Eds. (Springer New York, 2011), pp. 29–53.
112. J. T. Morton, S. D. Freed, S. W. Lee, I. Friedberg, A large scale prediction of bacteriocin gene blocks suggests a wide functional spectrum for bacteriocins. BMC Bioinformatics 16, 381 (2015). doi: 10.1186/s12859-015-0792-9; pmid: 26558535
113. E. Cascales et al., Colicin biology. Microbiol. Mol. Biol. Rev. 71, 158–229 (2007). doi: 10.1128/MMBR.00036-06; pmid: 17347522
114. M. Chatzidaki-Livanis et al., Gut symbiont Bacteroides fragilis secretes a eukaryotic-like ubiquitin protein that mediates intraspecies antagonism. MBio 8, e01902-17 (2017). doi: 10.1128/mBio.01902-17; pmid: 29184019
115. D. Scholl, Phage tail-like bacteriocins. Annu. Rev. Virol. 4, 453–467 (2017). doi: 10.1146/annurev-virology-101416-041632; pmid: 28961412
116. E. Grohmann, P. J. Christie, G. Waksman, S. Backert, Type IV secretion in Gram-negative and Gram-positive bacteria. Mol. Microbiol. 107, 455–471 (2018). doi: 10.1111/mmi.13896; pmid: 29235173
117. D. Zhang, R. F. de Souza, V. Anantharaman, L. M. Iyer, L. Aravind, Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol. Direct 7, 18 (2012). doi: 10.1186/1745-6150-7-18; pmid: 22731697
118. A. Jamet, X. Nassif, New players in the toxin field: Polymorphic toxin systems in bacteria. MBio 6, e00285–e15 (2015). doi: 10.1128/mBio.00285-15; pmid: 25944858
119. S. K. Aoki et al., Contact-dependent inhibition of growth in Escherichia coli. Science 309, 1245–1248 (2005). doi: 10.1126/science.1115109; pmid: 16109881
120. S. K. Aoki et al., A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468, 439–442 (2010). doi: 10.1038/nature09490; pmid: 21085179
121. J. S. Webb et al., Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition. PLOS ONE 8, e57609 (2013). doi: 10.1371/journal.pone.0057609; pmid: 23469034
122. Z. C. Ruhe, J. Y. Nguyen, C. M. Beck, D. A. Low, C. S. Hayes, The proton-motive force is required for translocation of CDI toxins across the inner membrane of target bacteria. Mol. Microbiol. 94, 466–481 (2014). doi: 10.1111/mmi.12779; pmid: 25174572
123. J. L. E. Willett, G. C. Gucinski, J. P. Fatherree, D. A. Low, C. S. Hayes, Contact-dependent growth inhibition toxins exploit multiple independent cell-entry pathways. Proc. Natl. Acad. Sci. U.S.A. 112, 11341–11346 (2015). doi: 10.1073/pnas.1512124112; pmid: 26305955
124. S. Koskiniemi et al., Rhs proteins from diverse bacteria mediate intercellular competition. Proc. Natl. Acad. Sci. U.S.A. 110, 7032–7037 (2013). doi: 10.1073/pnas.1300627110; pmid: 23572593
125. S. J. Foster, Molecular analysis of three major wall-associated proteins of Bacillus subtilis 168: Evidence for processing of the product of a gene encoding a 258 kDa precursor two-domain ligand-binding protein. Mol. Microbiol. 8, 299–310 (1993). doi: 10.1111/j.1365-2958.1993.tb01574.x; pmid: 8316082
126. F. Boyer, G. Fichant, J. Berthod, Y. Vandenbrouck, I. Attree, Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: What can be learned from available microbial genomic resources? BMC Genomics 10, 104 (2009). doi: 10.1186/1471-2164-10-104; pmid: 19284603
127. R. D. Hood et al., A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25–37 (2010). doi: 10.1016/j.chom.2009.12.007; pmid: 20114026
128. A. B. Russell et al., Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343–347 (2011). doi: 10.1038/nature10244; pmid: 21776080
129. J. C. Whitney et al., An interbacterial NAD(P)(+) glycohydrolase toxin requires elongation factor Tu for delivery to target cells. Cell 163, 607–619 (2015). doi: 10.1016/j.cell.2015.09.027; pmid: 26456113
130. A. B. Russell, S. B. Peterson, J. D. Mougous, Type VI secretion system effectors: Poisons with a purpose. Nat. Rev. Microbiol. 12, 137–148 (2014). doi: 10.1038/nrmicro3185; pmid: 24384601
131. J. Ma et al., PAAR-Rhs proteins harbor various C-terminal toxins to diversify the antibacterial pathways of type VI secretion systems. Environ. Microbiol. 19, 345–360 (2017). doi: 10.1111/1462-2920.13621; pmid: 27871130
132. M. Unnikrishnan, C. Constantinidou, T. Palmer, M. J. Pallen, The enigmatic Esx proteins: Looking beyond mycobacteria. Trends Microbiol. 25, 192–204 (2017). doi: 10.1016/j.tim.2016.11.004; pmid: 27894646
133. Z. Cao, M. G. Casabona, H. Kneuper, J. D. Chalmers, T. Palmer, The type VII secretion system of Staphylococcus aureus secretes a nuclease toxin that targets competitor bacteria. Nat. Microbiol. 2, 16183 (2016). doi: 10.1038/nmicrobiol.2016.183; pmid: 27723728
134. L. García-Bayona, M. S. Guo, M. T. Laub, Contact-dependent killing by Caulobacter crescentus via cell surface-associated, glycine zipper proteins. eLife 6, e24869 (2017). doi: 10.7554/eLife.24869; pmid: 28323618
135. E. Nudleman, D. Wall, D. Kaiser, Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309, 125–127 (2005). doi: 10.1126/science.1112440; pmid: 15994555
136. D. T. Pathak et al., Cell contact-dependent outer membrane exchange in myxobacteria: Genetic determinants and mechanism. PLOS Genet. 8, e1002626 (2012). doi: 10.1371/journal.pgen.1002626; pmid: 22511878