Type VI Secretion System Transports Zn to Combat Multiple Stresses and Host Immunity

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One unique feature of type VI secretion system is the presence of multiple distinct systems in certain bacterial species. It is well established that some of these systems function to compete for their living niches among diverse bacterial species, whilst the activity of many such transporters remains unknown. Because metal ions are essential components to virtually all forms of life including bacteria, eukaryotic hosts have evolved complicated strategies to sequester metal ions, which constitute a major branch of their nutritional immunity. Therefore the ability to acquire metal ions is critical for bacterial virulence. This study reveals that the T6SS-4 of Yersinia pseudotuberculosis (Yptb) functions to import Zn2+ from the environment to mitigate the detrimental effects such as hydroxyl radicals induced by diverse stresses. Expression of the transporter is activated by multiple regulatory proteins, including OxyR and OmpR that sense diverse environmental cues. Zinc ion acquisition is achieved by translocating a Zn2+-binding substrate YezP, which is co-regulated with T6SS-4 by OxyR. Our results reveal a novel role for type VI secretion system, which is important in the study of the mechanism of metal ion acquisition by bacteria and the role of this process in bacterial pathogenesis and survival in detrimental environments.

Vyšlo v časopise: Type VI Secretion System Transports Zn to Combat Multiple Stresses and Host Immunity. PLoS Pathog 11(7): e32767. doi:10.1371/journal.ppat.1005020
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005020

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Zdroje

1. Bingle LE, Bailey CM, Pallen MJ (2008) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11: 3–8. doi: 10.1016/j.mib.2008.01.006 18289922

2. Russell AB, Peterson SB, Mougous JD (2014) Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12: 137–148. doi: 10.1038/nrmicro3185 24384601

3. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I (2009) 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. doi: 10.1186/1471-2164-10-104 19284603

4. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 104: 15508–15513. 17873062

5. Chow J, Mazmanian SK (2010) A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 7: 265–276. doi: 10.1016/j.chom.2010.03.004 20413095

6. Burtnick MN, DeShazer D, Nair V, Gherardini FC, Brett PJ (2010) Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. Infect Immun 78: 88–99. doi: 10.1128/IAI.00985-09 19884331

7. Ma AT, Mekalanos JJ (2010) In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc Natl Acad Sci U S A 107: 4365–4370. doi: 10.1073/pnas.0915156107 20150509

8. Parsons DA, Heffron F (2005) sciS, an icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence. Infect Immun 73: 4338–4345. 15972528

9. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, et al. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475: 343–347. doi: 10.1038/nature10244 21776080

10. Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, et al. (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496: 508–512. doi: 10.1038/nature12074 23552891

11. Ma LS, Hachani A, Lin JS, Filloux A, Lai EM (2014) Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16: 94–104. doi: 10.1016/j.chom.2014.06.002 24981331

12. Weber B, Hasic M, Chen C, Wai SN, Milton DL (2009) Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environ Microbiol 11: 3018–3028. doi: 10.1111/j.1462-2920.2009.02005.x 19624706

13. Zhang W, Wang Y, Song Y, Wang T, Xu S, et al. (2013) A type VI secretion system regulated by OmpR in Yersinia pseudotuberculosis functions to maintain intracellular pH homeostasis. Environ Microbiol 15: 557–569. doi: 10.1111/1462-2920.12005 23094603

14. Gueguen E, Durand E, Zhang XY, d'Amalric Q, Journet L, et al. (2013) Expression of a type VI secretion system is responsive to envelope stresses through the OmpR transcriptional activator. PLoS One 8: e66615. 23840509

15. Storz G, Zheng M (2000) Bacterial Stress Responses; Storz G, Hengge-Aronis R, editors: American Society for Microbiology.

16. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755–776. doi: 10.1146/annurev.biochem.77.061606.161055 18173371

17. Mols M, Abee T (2011) Primary and secondary oxidative stress in Bacillus. Environ Microbiol 13: 1387–1394. doi: 10.1111/j.1462-2920.2011.02433.x 21352461

18. Ro SH, Nam M, Jang I, Park HW, Park H, et al. (2014) Sestrin2 inhibits uncoupling protein 1 expression through suppressing reactive oxygen species. Proc Natl Acad Sci U S A 111: 7849–7854. doi: 10.1073/pnas.1401787111 24825887

19. O'Donovan P, Perrett CM, Zhang X, Montaner B, Xu YZ, et al. (2005) Azathioprine and UVA light generate mutagenic oxidative DNA damage. Science 309: 1871–1874. 16166520

20. Dong TG, Dong S, Catalano C, Moore R, Liang X, et al. (2015) Generation of reactive oxygen species by lethal attacks from competing microbes. Proc Natl Acad Sci U S A 112: 2181–2186. doi: 10.1073/pnas.1425007112 25646446

21. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797–810. 17803904

22. Grant SS, Kaufmann BB, Chand NS, Haseley N, Hung DT (2012) Eradication of bacterial persisters with antibiotic-generated hydroxyl radicals. Proc Natl Acad Sci U S A 109: 12147–12152. doi: 10.1073/pnas.1203735109 22778419

23. Cornelis P, Wei Q, Andrews SC, Vinckx T (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 3: 540–549. doi: 10.1039/c1mt00022e 21566833

24. Anjem A, Varghese S, Imlay JA (2009) Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72: 844–858. doi: 10.1111/j.1365-2958.2009.06699.x 19400769

25. Gaballa A, Helmann JD (2002) A peroxide-induced zinc uptake system plays an important role in protection against oxidative stress in Bacillus subtilis. Mol Microbiol 45: 997–1005. 12180919

26. Mols M, van Kranenburg R, van Melis CC, Moezelaar R, Abee T (2010) Analysis of acid-stressed Bacillus cereus reveals a major oxidative response and inactivation-associated radical formation. Environ Microbiol 12: 873–885. doi: 10.1111/j.1462-2920.2009.02132.x 20074238

27. Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951–960. 15531603

28. Talmard C, Bouzan A, Faller P (2007) Zinc binding to amyloid-beta: isothermal titration calorimetry and Zn competition experiments with Zn sensors. Biochemistry 46: 13658–13666. 17983245

29. Hunt JB, Neece SH, Schachman HK, Ginsburg A (1984) Mercurial-promoted Zn2+ release from Escherichia coli aspartate transcarbamoylase. J Biol Chem 259: 14793–14803. 6389552

30. Perry RD, Fetherston JD (2011) Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect 13: 808–817. doi: 10.1016/j.micinf.2011.04.008 21609780

31. Bergman MA, Loomis WP, Mecsas J, Starnbach MN, Isberg RR (2009) CD8+ T cells restrict Yersinia pseudotuberculosis infection: bypass of anti-phagocytosis by targeting antigen-presenting cells. PLoS Pathog 5: e1000573. doi: 10.1371/journal.ppat.1000573 19730693

32. Oteiza PI (2012) Zinc and the modulation of redox homeostasis. Free Radic Biol Med 53: 1748–1759. doi: 10.1016/j.freeradbiomed.2012.08.568 22960578

33. Isohanni P, Huehn S, Aho T, Alter T, Lyhs U (2013) Heat stress adaptation induces cross-protection against lethal acid stress conditions in Arcobacter butzleri but not in Campylobacter jejuni. Food Microbiol 34: 431–435. doi: 10.1016/j.fm.2013.02.001 23541213

34. Porcheron G, Garenaux A, Proulx J, Sabri M, Dozois CM (2013) Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front Cell Infect Microbiol 3: 90. doi: 10.3389/fcimb.2013.00090 24367764

35. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71: 413–451. 17804665

36. Hood MI, Skaar EP (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525–537. doi: 10.1038/nrmicro2836 22796883

37. Cerasi M, Ammendola S, Battistoni A (2013) Competition for zinc binding in the host-pathogen interaction. Front Cell Infect Microbiol 3: 108. doi: 10.3389/fcimb.2013.00108 24400228

38. Hood MI, Mortensen BL, Moore JL, Zhang Y, Kehl-Fie TE, et al. (2012) Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog 8: e1003068. doi: 10.1371/journal.ppat.1003068 23236280

39. Yang X, Becker T, Walters N, Pascual DW (2006) Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect Immun 74: 3874–3879. 16790759

40. Davis LM, Kakuda T, DiRita VJ (2009) A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol 191: 1631–1640. doi: 10.1128/JB.01394-08 19103921

41. Desrosiers DC, Bearden SW, Mier I Jr., Abney J, Paulley JT, et al. (2010) Znu is the predominant zinc importer in Yersinia pestis during in vitro growth but is not essential for virulence. Infect Immun 78: 5163–5177. doi: 10.1128/IAI.00732-10 20855510

42. Bobrov AG, Kirillina O, Fetherston JD, Miller MC, Burlison JA, et al. (2014) The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicaemic plague in mice. Mol Microbiol 93: 759–775. doi: 10.1111/mmi.12693 24979062

43. Heroven AK, Bohme K, Tran-Winkler H, Dersch P (2007) Regulatory elements implicated in the environmental control of invasin expression in enteropathogenic Yersinia. Adv Exp Med Biol 603: 156–166. 17966412

44. Cortese MS, Paszczynski A, Lewis TA, Sebat JL, Borek V, et al. (2002) Metal chelating properties of pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas spp. and the biological activities of the formed complexes. Biometals 15: 103–120. 12046919

45. Citiulo F, Jacobsen ID, Miramon P, Schild L, Brunke S, et al. (2012) Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog 8: e1002777. doi: 10.1371/journal.ppat.1002777 22761575

46. Serafini A, Boldrin F, Palu G, Manganelli R (2009) Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J Bacteriol 191: 6340–6344. doi: 10.1128/JB.00756-09 19684129

47. Yatsunyk LA, Easton JA, Kim LR, Sugarbaker SA, Bennett B, et al. (2008) Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli. J Biol Inorg Chem 13: 271–288. 18027003

48. Simons TJ (1993) Measurement of free Zn2+ ion concentration with the fluorescent probe mag-fura-2 (furaptra). J Biochem Biophys Methods 27: 25–37. 8409208

49. Chao Y, Fu D (2004) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279: 17173–17180. 14960568

50. Russell D, Soulimane T (2012) Evidence for zinc and cadmium binding in a CDF transporter lacking the cytoplasmic domain. FEBS Lett 586: 4332–4338. doi: 10.1016/j.febslet.2012.10.043 23127559

51. Tanaka N, Kawachi M, Fujiwara T, Maeshima M (2013) Zinc-binding and structural properties of the histidine-rich loop of Arabidopsis thaliana vacuolar membrane zinc transporter MTP1. FEBS Open Bio 3: 218–224. doi: 10.1016/j.fob.2013.04.004 23772397

52. Zhang W, Xu S, Li J, Shen X, Wang Y, et al. (2011) Modulation of a thermoregulated type VI secretion system by AHL-dependent quorum sensing in Yersinia pseudotuberculosis. Arch Microbiol 193: 351–363. doi: 10.1007/s00203-011-0680-2 21298257

53. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254. 942051

54. Aldridge PD, Karlinsey JE, Aldridge C, Birchall C, Thompson D, et al. (2006) The flagellar-specific transcription factor, σ28, is the Type III secretion chaperone for the flagellar-specific anti-σ28 factor FlgM. Genes Dev 20: 2315–2326. 16912280

55. Xu L, Shen X, Bryan A, Banga S, Swanson MS, et al. (2010) Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog 6: e1000822. doi: 10.1371/journal.ppat.1000822 20333253

56. Miller JH (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.

57. Wang Y, Cen XF, Zhao GP, Wang J (2012) Characterization of a new GlnR binding box in the promoter of amtB in Streptomyces coelicolor inferred a PhoP/GlnR competitive binding mechanism for transcriptional regulation of amtB. J Bacteriol 194: 5237–5244. doi: 10.1128/JB.00989-12 22821977

58. Puri S, Hohle TH, O'Brian MR (2010) Control of bacterial iron homeostasis by manganese. Proc Natl Acad Sci U S A 107: 10691–10695. doi: 10.1073/pnas.1002342107 20498065

59. Champion OL, Karlyshev A, Cooper IA, Ford DC, Wren BW, et al. (2011) Yersinia pseudotuberculosis mntH functions in intracellular manganese accumulation, which is essential for virulence and survival in cells expressing functional Nramp1. Microbiology 157: 1115–1122. doi: 10.1099/mic.0.045807-0 21183572

60. Schilling O, Vogel A, Kostelecky B, Natal da Luz H, Spemann D, et al. (2005) Zinc- and iron-dependent cytosolic metallo-beta-lactamase domain proteins exhibit similar zinc-binding affinities, independent of an atypical glutamate at the metal-binding site. Biochem J 385: 145–153. 15324305

61. Saraswathi R, Pait Chowdhury R, Williams SM, Ghatak P, Chatterji D (2009) The mycobacterial MsDps2 protein is a nucleoid-forming DNA binding protein regulated by sigma factors σA and σB. PLoS One 4: e8017. doi: 10.1371/journal.pone.0008017 19956571

62. Liu Y, Luo ZQ (2007) The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun 75: 592–603. 17101649

63. Heroven AK, Sest M, Pisano F, Scheb-Wetzel M, Steinmann R, et al. (2012) Crp induces switching of the CsrB and CsrC RNAs in Yersinia pseudotuberculosis and links nutritional status to virulence. Front Cell Infect Microbiol 2: 158. doi: 10.3389/fcimb.2012.00158 23251905

64. Schweer J, Kulkarni D, Kochut A, Pezoldt J, Pisano F, et al. (2013) The cytotoxic necrotizing factor of Yersinia pseudotuberculosis (CNFY) enhances inflammation and Yop delivery during infection by activation of Rho GTPases. PLoS Pathog 9: e1003746. doi: 10.1371/journal.ppat.1003746 24244167