Attenuation of the Sensing Capabilities of PhoQ in Transition to Obligate Insect–Bacterial Association
Sodalis glossinidius, a maternally inherited endosymbiont of the tsetse fly, maintains genes encoding homologues of the PhoP-PhoQ two-component regulatory system. This two-component system has been extensively studied in facultative bacterial pathogens and is known to serve as an environmental magnesium sensor and a regulator of key virulence determinants. In the current study, we show that the inactivation of the response regulator, phoP, renders S. glossinidius sensitive to insect derived cationic antimicrobial peptides (AMPs). The resulting mutant strain displays reduced expression of genes involved in the structural modification of lipid A that facilitates resistance to AMPs. In addition, the inactivation of phoP alters the expression of type-III secretion system (TTSS) genes encoded within three distinct chromosomal regions, indicating that PhoP-PhoQ also serves as a master regulator of TTSS gene expression. In the absence of phoP, S. glossinidius is unable to superinfect either its natural tsetse fly host or a closely related hippoboscid louse fly. Furthermore, we show that the S. glossinidius PhoQ sensor kinase has undergone functional adaptations that result in a substantially diminished ability to sense ancestral signals. The loss of PhoQ's sensory capability is predicted to represent a novel adaptation to the static symbiotic lifestyle, allowing S. glossinidius to constitutively express genes that facilitate resistance to host derived AMPs.
Vyšlo v časopise:
Attenuation of the Sensing Capabilities of PhoQ in Transition to Obligate Insect–Bacterial Association. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002349
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002349
Souhrn
Sodalis glossinidius, a maternally inherited endosymbiont of the tsetse fly, maintains genes encoding homologues of the PhoP-PhoQ two-component regulatory system. This two-component system has been extensively studied in facultative bacterial pathogens and is known to serve as an environmental magnesium sensor and a regulator of key virulence determinants. In the current study, we show that the inactivation of the response regulator, phoP, renders S. glossinidius sensitive to insect derived cationic antimicrobial peptides (AMPs). The resulting mutant strain displays reduced expression of genes involved in the structural modification of lipid A that facilitates resistance to AMPs. In addition, the inactivation of phoP alters the expression of type-III secretion system (TTSS) genes encoded within three distinct chromosomal regions, indicating that PhoP-PhoQ also serves as a master regulator of TTSS gene expression. In the absence of phoP, S. glossinidius is unable to superinfect either its natural tsetse fly host or a closely related hippoboscid louse fly. Furthermore, we show that the S. glossinidius PhoQ sensor kinase has undergone functional adaptations that result in a substantially diminished ability to sense ancestral signals. The loss of PhoQ's sensory capability is predicted to represent a novel adaptation to the static symbiotic lifestyle, allowing S. glossinidius to constitutively express genes that facilitate resistance to host derived AMPs.
Zdroje
1. DaleCMoranNA 2006 Molecular interactions between bacterial symbionts and their hosts. Cell 126 453 465
2. BlattnerFRPlunkett G3rdBlochCAPernaNTBurlandV 1997 The complete genome sequence of Escherichia coli K-12. Science 277 1453 1474
3. ChenXALiSAksoyS 1999 Concordant evolution of a symbiont with its host insect species: Molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48 49 58
4. ThomsonNRHowardSWrenBWHoldenMTCrossmanL 2006 The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2 e206 doi:10.1371/journal.pgen.0020206
5. TohHWeissBLPerkinSAYamashitaAOshimaK 2006 Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16 149 156
6. DaleCYoungSAHaydonDTWelburnSC 2001 The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci U S A 98 1883 1888
7. DaleCPlagueGRWangBOchmanHMoranNA 2002 Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci U S A 99 12397 12402
8. DaleCJonesTPontesM 2005 Degenerative evolution and functional diversification of type-III secretion systems in the insect endosymbiont Sodalis glossinidius. Mol Biol Evol 22 758 766
9. MoranNADegnanPHSantosSRDunbarHEOchmanH 2005 The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci U S A 102 16919 16926
10. NovákováEHypsaV 2007 A new Sodalis lineage from bloodsucking fly Craterina melbae (Diptera, Hippoboscoidea) originated independently of the tsetse flies symbiont Sodalis glossinidius. FEMS Microbiol Lett 269 131 135
11. DegnanPHYuYSisnerosNWingRAMoranNA 2009 Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci U S A 106 9063 9068
12. DerzelleSTurlinEDuchaudEPagesSKunstF 2004 The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186 1270 1279
13. GroismanEA 2001 The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183 1835 1842
14. PerezJCShinDZwirILatifiTHadleyTJ 2009 Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet 5 e1000428 doi:10.1371/journal.pgen.1000428
15. GroismanEAMouslimC 2006 Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 4 705 709
16. MitrophanovAYJewettMWHadleyTJGroismanEA 2008 Evolution and dynamics of regulatory architectures controlling polymyxin B resistance in enteric bacteria. PLoS Genet 4 e1000233 doi:10.1371/journal.pgen.1000233
17. BaderMWSanowarSDaleyMESchneiderARChoU 2005 Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122 461 472
18. ProstLRDaleyMELe SageVBaderMWLe MoualH 2007 Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26 165 174
19. Guaní-GuerraESantos-MendozaTLugo-ReyesSOTeránLM 2010 Antimicrobial peptides: general overview and clinical implications in human health and disease. Clin Immunol 135 1 11
20. LemaitreBHoffmannJ 2007 The host defense of Drosophila melanogaster. Annu Rev Immunol 25 697 743
21. DaleCBeetonMHarbisonCJonesTPontesM 2006 Isolation, pure culture, and characterization of “Candidatus Arsenophonus arthropodicus,” an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 72 2997 3004
22. HainesLRHancockREPearsonTW 2003 Cationic antimicrobial peptide killing of African trypanosomes and Sodalis glossinidius, a bacterial symbiont of the insect vector of sleeping sickness. Vector Borne Zoonotic Dis 3 175 186
23. HaoZKasumbaILehaneMJGibsonWCKwonJ 2001 Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proc Natl Acad Sci U S A 98 12648 12653
24. PontesMHDaleC 2011 Lambda Red-mediated genetic modification of the insect endosymbiont Sodalis glossinidius. Appl Environ Microbiol 77 1918 1920
25. AkodaKVan den BosschePMarcottyTKubiCCoosemansM 2009 Nutritional stress affects the tsetse fly's immune gene expression. Med Vet Entomol 23 195 201
26. BoulangerNBrunREhret-SabatierLKunzCBuletP 2002 Immunepeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Biochem Mol Biol 32 369 375
27. ShiYCromieMJHsuFFTurkJGroismanEA 2004 PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol Microbiol 53 229 241
28. GunnJS 2008 The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol 16 284 290
29. MinagawaSOgasawaraHKatoAYamamotoKEguchiY 2003 Identification and molecular characterization of the Mg2+ stimulon of Escherichia coli. J Bacteriol 185 3696 3702
30. ZwirIShinDKatoANishinoKLatifiT 2005 Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci USA 102 2862 2867
31. BajajVLucasRLHwangCLeeCA 1996 Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22 703 714
32. ChengQAksoyS 1999 Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol 8 125 132
33. PontesMHDaleC 2006 Culture and manipulation of insect facultative symbionts. Trends Microbiol 14 406 412
34. WeissBLWuYSchwankJJTolwinskiNSAksoyS 2008 An insect symbiosis is influenced by bacterium-specific polymorphisms in outer-membrane protein A. Proc Natl Acad Sci USA 105 15088 15093
35. WeissBLWangJAksoyS 2011 Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol 9 e1000619 doi:10.1371/journal.pbio.1000619
36. PetersenFTMeierRKuttySNWiegmannBM 2007 The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Mol Phylogenet Evol 45 111 122
37. García VéscoviESonciniFCGroismanEA 1996 Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84 165 174
38. ChamnongpolSCromieMGroismanEA 2003 Mg2+ sensing by the Mg2+ sensor PhoQ of Salmonella enterica. J Mol Biol 325 795 807
39. ChamnongpolSGroismanEA 2000 Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase. J Mol Biol 300 291 305
40. SnavelyMDMillerCGMaguireME 1991 The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266 815 823
41. TaoTSnavelyMDFarrSGMaguireME 1995 Magnesium transport in Salmonella typhimurium: mgtA encodes a P-type ATPase and is regulated by Mg2+ in a manner similar to that of the mgtB P-type ATPase. J Bacteriol 177 2654 2662
42. DaleCMaudlinI 1999 Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol 49 267 275
43. MillerSIMekalanosJJ 1990 Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol. 172 2485 2490
44. ShinDLeeEJHuangHGroismanEA 2006 A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circuit. Science 314 1607 1609
45. NatochinYVParnovaRG 1987 Osmolality and electrolyte concentration of hemolymph and the problem of ion and volume regulation of cells in higher insects. Comp Biochem Physiol A 88 563 570
46. PetitJP 1968 Hemolymph of Glossina: collection and analysis. Rev Elev Med Vet Pays Trop 21 493 498
47. ChoUSBaderMWAmayaMFDaleyMEKlevitRE 2006 Metal bridges between the PhoQ sensor domain and the membrane regulate transmembrane signaling. J Mol Biol 356 1193 1206
48. ChakrabortySLiMChatterjeeCSivaramanJLeungKY 2010 Temperature and Mg2+ sensing by a novel PhoP-PhoQ two-component system for regulation of virulence in Edwardsiella tarda. J Biol Chem 285 38876 38888
49. FukatsuTKogaRSmithWATanakaKNikohN 2007 Bacterial endosymbiont of the slender pigeon louse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl Environ Microbiol 73 6660 6668
50. KaiwaNHosokawaTKikuchiYNikohNMengXY 2010 Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol 76 3486 3494
51. NovákováEHypsaVMoranNA 2009 Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9 143
52. DatsenkoKAWannerBL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97 6640 6645
53. InoueHNojimaHOkayamaH 1990 High efficiency transformation of Escherichia coli with plasmids. Gene 96 23 28
54. GroismanEAHeffronFSolomonF 1992 Molecular genetic analysis of the Escherichia coli phoP locus. J Bacteriol 174 486 491
55. SonciniFCVéscoviEGGroismanEA 1995 Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177 4364 4371
56. MillerJH 1992 A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. New York Cold Spring Harbor Laboratory Press 456
57. MatyashVLiebischGKurzchaliaTVShevchenkoASchwudkeD 2008 Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. J Lipid Res 49 1137 1146
58. GosalbesMJLatorreALamelasAMoyaA 2010 Genomics of intracellular symbionts in insects. Int J Med Microbiol 300 271 278
59. KatohKMisawaKKumaKMiyataT 2002 MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acid Res 30 3059 3066
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 11
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Evidence-Based Annotation of Gene Function in MR-1 Using Genome-Wide Fitness Profiling across 121 Conditions
- De Novo Origins of Human Genes
- TRY-5 Is a Sperm-Activating Protease in Seminal Fluid
- Relative Burden of Large CNVs on a Range of Neurodevelopmental Phenotypes