The Toxin/immunity Network of Burkholderia Pseudomallei Contact-dependent Growth Inhibition (CDI) Systems

Overview

Journal Mol Microbiol

Specialties Microbiology
Molecular Biology

Date 2012 Mar 23

PMID 22435733

Citations 70

Authors

Kiel Nikolakakis

Saba Amber

J Scott Wilbur

Elie J Diner

Stephanie K Aoki

Stephen J Poole

Apichai Tuanyok

Paul S Keim

Sharon Peacock

Christopher S Hayes

David A Low

Affiliations

Soon will be listed here.

Abstract

Burkholderia pseudomallei is a category B pathogen and the causative agent of melioidosis--a serious infectious disease that is typically acquired directly from environmental reservoirs. Nearly all B. pseudomallei strains sequenced to date (> 85 isolates) contain gene clusters that are related to the contact-dependent growth inhibition (CDI) systems of γ-proteobacteria. CDI systems from Escherichia coli and Dickeya dadantii play significant roles in bacterial competition, suggesting these systems may also contribute to the competitive fitness of B. pseudomallei. Here, we identify 10 distinct CDI systems in B. pseudomallei based on polymorphisms within the cdiA-CT/cdiI coding regions, which are predicted to encode CdiA-CT/CdiI toxin/immunity protein pairs. Biochemical analysis of three B. pseudomallei CdiA-CTs revealed that each protein possesses a distinct tRNase activity capable of inhibiting cell growth. These toxin activities are blocked by cognate CdiI immunity proteins, which specifically bind the CdiA-CT and protect cells from growth inhibition. Using Burkholderia thailandensis E264 as a model, we show that a CDI system from B. pseudomallei 1026b mediates CDI and is capable of delivering CdiA-CT toxins derived from other B. pseudomallei strains. These results demonstrate that Burkholderia species contain functional CDI systems, which may confer a competitive advantage to these bacteria.

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References

Chantratita N, Wuthiekanun V, Limmathurotsakul D, Vesaratchavest M, Thanwisai A, Amornchai P . Genetic diversity and microevolution of Burkholderia pseudomallei in the environment. PLoS Negl Trop Dis. 2008; 2(2):e182. PMC: 2254201. DOI: 10.1371/journal.pntd.0000182. View

Kang Y, Norris M, Wilcox B, Tuanyok A, Keim P, Hoang T . Knockout and pullout recombineering for naturally transformable Burkholderia thailandensis and Burkholderia pseudomallei. Nat Protoc. 2011; 6(8):1085-104. PMC: 3564556. DOI: 10.1038/nprot.2011.346. View

Ogawa T, Tomita K, Ueda T, Watanabe K, Uozumi T, Masaki H . A cytotoxic ribonuclease targeting specific transfer RNA anticodons. Science. 1999; 283(5410):2097-100. DOI: 10.1126/science.283.5410.2097. View

Buscher A, Grass S, Heuser J, Roth R, St Geme 3rd J . Surface anchoring of a bacterial adhesin secreted by the two-partner secretion pathway. Mol Microbiol. 2006; 61(2):470-83. DOI: 10.1111/j.1365-2958.2006.05236.x. View

Mazar J, Cotter P . New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol. 2007; 15(11):508-15. DOI: 10.1016/j.tim.2007.10.005. View

Choi K, Gaynor J, White K, Lopez C, Bosio C, Karkhoff-Schweizer R . A Tn7-based broad-range bacterial cloning and expression system. Nat Methods. 2005; 2(6):443-8. DOI: 10.1038/nmeth765. View

Wah D, Levchenko I, Rieckhof G, Bolon D, Baker T, Sauer R . Flexible linkers leash the substrate binding domain of SspB to a peptide module that stabilizes delivery complexes with the AAA+ ClpXP protease. Mol Cell. 2003; 12(2):355-63. DOI: 10.1016/s1097-2765(03)00272-7. View

Garza-Sanchez F, Janssen B, Hayes C . Prolyl-tRNA(Pro) in the A-site of SecM-arrested ribosomes inhibits the recruitment of transfer-messenger RNA. J Biol Chem. 2006; 281(45):34258-68. PMC: 2777889. DOI: 10.1074/jbc.M608052200. View

Tomita K, Ogawa T, Uozumi T, Watanabe K, Masaki H . A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proc Natl Acad Sci U S A. 2000; 97(15):8278-83. PMC: 26938. DOI: 10.1073/pnas.140213797. View

10.

Brett P, Deshazer D, Woods D . Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol. 1998; 48 Pt 1:317-20. DOI: 10.1099/00207713-48-1-317. View

11.

Tomich M, Herfst C, Golden J, Mohr C . Role of flagella in host cell invasion by Burkholderia cepacia. Infect Immun. 2002; 70(4):1799-806. PMC: 127839. DOI: 10.1128/IAI.70.4.1799-1806.2002. View

12.

Choi K, DeShazer D, Schweizer H . mini-Tn7 insertion in bacteria with multiple glmS-linked attTn7 sites: example Burkholderia mallei ATCC 23344. Nat Protoc. 2007; 1(1):162-9. DOI: 10.1038/nprot.2006.25. View

13.

Lazar Adler N, Govan B, Cullinane M, Harper M, Adler B, Boyce J . The molecular and cellular basis of pathogenesis in melioidosis: how does Burkholderia pseudomallei cause disease?. FEMS Microbiol Rev. 2009; 33(6):1079-99. DOI: 10.1111/j.1574-6976.2009.00189.x. View

14.

Michel-Briand Y, Baysse C . The pyocins of Pseudomonas aeruginosa. Biochimie. 2002; 84(5-6):499-510. DOI: 10.1016/s0300-9084(02)01422-0. View

15.

Aiyar A, Xiang Y, Leis J . Site-directed mutagenesis using overlap extension PCR. Methods Mol Biol. 1996; 57:177-91. DOI: 10.1385/0-89603-332-5:177. View

16.

Boonbumrung K, Wuthiekanun V, Rengpipat S, Day N, Peacock S . In vitro motility of a population of clinical Burkholderia pseudomallei isolates. J Med Assoc Thai. 2006; 89(9):1506-10. View

17.

Limmathurotsakul D, Peacock S . Melioidosis: a clinical overview. Br Med Bull. 2011; 99:125-39. DOI: 10.1093/bmb/ldr007. View

18.

Hayes C, Aoki S, Low D . Bacterial contact-dependent delivery systems. Annu Rev Genet. 2010; 44:71-90. DOI: 10.1146/annurev.genet.42.110807.091449. View

19.

Wuthiekanun V, Limmathurotsakul D, Chantratita N, Feil E, Day N, Peacock S . Burkholderia Pseudomallei is genetically diverse in agricultural land in Northeast Thailand. PLoS Negl Trop Dis. 2009; 3(8):e496. PMC: 2713400. DOI: 10.1371/journal.pntd.0000496. View

20.

Wah D, Levchenko I, Baker T, Sauer R . Characterization of a specificity factor for an AAA+ ATPase: assembly of SspB dimers with ssrA-tagged proteins and the ClpX hexamer. Chem Biol. 2002; 9(11):1237-45. DOI: 10.1016/s1074-5521(02)00268-5. View