Contact-dependent growth inhibition toxins exploit multiple independent cell-entry pathways

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 36, 2015, Pages 11341-11346

  Willett, Julia L E ^a   Gucinski, Grant C ^a   Fatherree, Jackson P ^a   Low, David A ^a   Hayes, Christopher S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bacterial cell envelope; Dnase activity; Genetic selection; Toxin immunity genes; Trnase activity

Indexed keywords

MEMBRANE PROTEIN; TOXIN; BACTERIAL TOXIN; CDIA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BURKHOLDERIA PSEUDOMALLEI; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; CELL SURFACE; CELL TRANSPORT; CONTACT DEPENDENT GROWTH INHIBITION SYSTEM; CYTOPLASM; ESCHERICHIA COLI; GROWTH INHIBITION; INNER MEMBRANE; MUTAGENESIS; MUTATION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN TRANSPORT; TARGET CELL; YERSINIA PESTIS; AMINO ACID SEQUENCE; BACTERIUM ADHERENCE; BINDING SITE; CLASSIFICATION; CONTACT INHIBITION; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; BACTERIAL ADHESION; BACTERIAL TOXINS; BINDING SITES; CONTACT INHIBITION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84941254140     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1512124112     Document Type: Article

References (44)

1. Ruhe ZC, Low DA, Hayes CS (2013) Bacterial contact-dependent growth inhibition. Trends Microbiol 21(5):230-237.
2. Silverman JM, Brunet YR, Cascales E, Mougous JD (2012) Structure and regulation of the type VI secretion system. Annu Rev Microbiol 66:453-472.
3. Aoki SK, et al. (2008) Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 70(2):323-340.
4. Aoki SK, et al. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309(5738):1245-1248.
5. Kajava AV, et al. (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42(2):279-292.
6. Aoki SK, et al. (2010) A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468(7322):439-442.
7. Ruhe ZC, Wallace AB, Low DA, Hayes CS (2013) Receptor polymorphism restricts contact-dependent growth inhibition to members of the same species. MBio 4(4):e00480-e00413.
8. Nikolakakis K, et al. (2012) The toxin/immunity network of Burkholderia pseudomallei contact-dependent growth inhibition (CDI) systems. Mol Microbiol 84(3):516-529.
9. Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L (2012) Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 7:18.
10. Beck CM, et al. (2014) CdiA from Enterobacter cloacae delivers a toxic ribosomal RNase into target bacteria. Structure 22(5):707-718.
11. Morse RP, et al. (2012) Structural basis of toxicity and immunity in contact-dependent growth inhibition (CDI) systems. Proc Natl Acad Sci USA 109(52):21480-21485.
12. Ruhe ZC, Nguyen JY, Beck CM, Low DA, Hayes CS (2014) The proton-motive force is required for translocation of CDI toxins across the inner membrane of target bacteria. Mol Microbiol 94(2):466-481.
13. Webb JS, et al. (2013) Delivery of CdiA nuclease toxins into target cells during contactdependent growth inhibition. PLoS One 8(2):e57609.
14. Diner EJ, Beck CM, Webb JS, Low DA, Hayes CS (2012) Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes Dev 26(5):515-525.
15. Stewart JB, Hermodson MA (2003) Topology of RbsC, the membrane component of the Escherichia coli ribose transporter. J Bacteriol 185(17):5234-5239.
16. Gál J, Szvetnik A, Schnell R, Kálmán M (2002) The metD D-methionine transporter locus of Escherichia coli is an ABC transporter gene cluster. J Bacteriol 184(17):4930-4932.
17. Merlin C, Gardiner G, Durand S, Masters M (2002) The Escherichia coli metD locus encodes an ABC transporter which includes Abc (MetN), YaeE (MetI), and YaeC (MetQ). J Bacteriol 184(19):5513-5517.
18. Buhr A, Flükiger K, Erni B (1994) The glucose transporter of Escherichia coli. Overexpression, purification, and characterization of functional domains. J Biol Chem 269(38):23437-23443.
19. McGinness KE, Baker TA, Sauer RT (2006) Engineering controllable protein degradation. Mol Cell 22(5):701-707.
20. Poole SJ, et al. (2011) Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7(8):e1002217.
21. Meins M, et al. (1993) Cysteine phosphorylation of the glucose transporter of Escherichia coli. J Biol Chem 268(16):11604-11609.
22. Qu JN, et al. (1996) The tolZ gene of Escherichia coli is identified as the ftsH gene. J Bacteriol 178(12):3457-3461.
23. Chauleau M, Mora L, Serba J, de Zamaroczy M (2011) FtsH-dependent processing of RNasecolicins D and E3 means that only the cytotoxic domains are imported into the cytoplasm. J Biol Chem 286(33):29397-29407.
24. Walker D, Mosbahi K, Vankemmelbeke M, James R, Kleanthous C (2007) The role of electrostatics in colicin nuclease domain translocation into bacterial cells. J Biol Chem 282(43):31389-31397.
25. 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(8):e1002877.
26. Koskiniemi S, et al. (2015) Genetic analysis of the CDI pathway from Burkholderia pseudomallei 1026b. PLoS One 10(3):e0120265.
27. Law CJ, Maloney PC, Wang DN (2008) Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 62:289-305.
28. Mosbahi K, et al. (2002) The cytotoxic domain of colicin E9 is a channel-forming endonuclease. Nat Struct Biol 9(6):476-484.
29. Mosbahi K, Walker D, James R, Moore GR, Kleanthous C (2006) Global structural rearrangement of the cell penetrating ribonuclease colicin E3 on interaction with phospholipid membranes. Protein Sci 15(3):620-627.
30. Sharma O, et al. (2009) Genome-wide screens: Novel mechanisms in colicin import and cytotoxicity. Mol Microbiol 73(4):571-585.
31. Teff D, Koby S, Shotland Y, Ogura T, Oppenheim AB (2000) A colicin-tolerant Escherichia coli mutant that confers hflphenotype carries two mutations in the region coding for the C-terminal domain of FtsH (HflB). FEMS Microbiol Lett 183(1):115-117.
32. Mora L, de Zamaroczy M (2014) In vivo processing of DNase colicins E2 and E7 is required for their import into the cytoplasm of target cells. PLoS One 9(5):e96549.
33. Williams N, Fox DK, Shea C, Roseman S (1986) Pel, the protein that permits lambda DNA penetration of Escherichia coli, is encoded by a gene in ptsM and is required for mannose utilization by the phosphotransferase system. Proc Natl Acad Sci USA 83(23):8934-8938.
34. Cumby N, Reimer K, Mengin-Lecreulx D, Davidson AR, Maxwell KL (2015) The phage tail tape measure protein, an inner membrane protein and a periplasmic chaperone play connected roles in the genome injection process of E. coli phage HK97. Mol Microbiol 96(3):437-447.
35. Jamet A, et al. (2015) A new family of secreted toxins in pathogenic Neisseria species. PLoS Pathog 11(1):e1004592.
36. Koskiniemi S, et al. (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 110(17):7032-7037.
37. Holberger LE, Garza-Sánchez F, Lamoureux J, Low DA, Hayes CS (2012) A novel family of toxin/antitoxin proteins in Bacillus species. FEBS Lett 586(2):132-136.
38. Chiang SL, Rubin EJ (2002) Construction of a mariner-based transposon for epitopetagging and genomic targeting. Gene 296(1-2):179-185.
39. Baba T, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2:2006.0008.
40. (Pro) in the A-site of SecMarrested ribosomes inhibits the recruitment of transfer-messenger RNA. J Biol Chem 281(45):34258-34268.
41. Datta S, Costantino N, Court DL (2006) A set of recombineering plasmids for gramnegative bacteria. Gene 379:109-115.
42. Schindelin J, et al. (2012) Fiji: An open-source platform for biological-image analysis. Nat Methods 9(7):676-682.
43. Ferrières L, et al. (2010) Silent mischief: Bacteriophage Mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. J Bacteriol 192(24):6418-6427.
44. Akiyama Y, Shirai Y, Ito K (1994) Involvement of FtsH in protein assembly into and through the membrane. II. Dominant mutations affecting FtsH functions. J Biol Chem 269(7):5225-5229.