Academic Journal
Silencing urease: a key evolutionary step that facilitated the adaptation of Yersinia pestis to the flea-borne transmission route.
| Τίτλος: | Silencing urease: a key evolutionary step that facilitated the adaptation of Yersinia pestis to the flea-borne transmission route. |
|---|---|
| Συγγραφείς: | Chouikha I; Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840 iman.chouikha@nih.gov., Hinnebusch BJ; Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840. |
| Πηγή: | Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2014 Dec 30; Vol. 111 (52), pp. 18709-14. Date of Electronic Publication: 2014 Dec 01. |
| Τύπος έκδοσης: | Journal Article; Research Support, N.I.H., Intramural |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: National Academy of Sciences Country of Publication: United States NLM ID: 7505876 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1091-6490 (Electronic) Linking ISSN: 00278424 NLM ISO Abbreviation: Proc Natl Acad Sci U S A Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Washington, DC : National Academy of Sciences |
| Ιατρικοί όροι (MeSH): | Bacterial Proteins*/genetics , Bacterial Proteins*/metabolism , Urease*/genetics , Urease*/metabolism , Yersinia pestis*/enzymology , Yersinia pestis*/genetics , Yersinia pestis*/pathogenicity , Evolution, Molecular* , Gene Silencing*, Insect Vectors/*microbiology , Xenopsylla/*microbiology, Plague/enzymology ; Plague/genetics ; Plague/pathology ; Plague/transmission ; Yersinia pseudotuberculosis/enzymology ; Yersinia pseudotuberculosis/genetics ; Yersinia pseudotuberculosis/pathogenicity ; Animals ; Humans ; Mutation |
| Περίληψη: | The arthropod-borne transmission route of Yersinia pestis, the bacterial agent of plague, is a recent evolutionary adaptation. Yersinia pseudotuberculosis, the closely related food-and water-borne enteric species from which Y. pestis diverged less than 6,400 y ago, exhibits significant oral toxicity to the flea vectors of plague, whereas Y. pestis does not. In this study, we identify the Yersinia urease enzyme as the responsible oral toxin. All Y. pestis strains, including those phylogenetically closest to the Y. pseudotuberculosis progenitor, contain a mutated ureD allele that eliminated urease activity. Restoration of a functional ureD was sufficient to make Y. pestis orally toxic to fleas. Conversely, deletion of the urease operon in Y. pseudotuberculosis rendered it nontoxic. Enzymatic activity was required for toxicity. Because urease-related mortality eliminates 30-40% of infective flea vectors, ureD mutation early in the evolution of Y. pestis was likely subject to strong positive selection because it significantly increased transmission potential. |
| Σχόλια: | Comment in: Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18409-10. doi: 10.1073/pnas.1421887112.. (PMID: 25535337) |
| References: | Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13826-31. (PMID: 15358858) J Hyg (Lond). 1914 Jan;13(Suppl):423-39. (PMID: 20474555) Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):577-82. (PMID: 23271803) Arch Insect Biochem Physiol. 2000 Aug;44(4):162-71. (PMID: 10918311) Infect Immun. 1997 May;65(5):1985-90. (PMID: 9125594) Infect Immun. 2007 Feb;75(2):774-80. (PMID: 17101645) Science. 2002 Apr 26;296(5568):733-5. (PMID: 11976454) Eur J Clin Microbiol Infect Dis. 1999 Jan;18(1):1-15. (PMID: 10192708) Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6236-41. (PMID: 16603630) Metallomics. 2009;1(3):207-21. (PMID: 20046957) J Biol Chem. 2013 May 10;288(19):13178-85. (PMID: 23539618) J Econ Entomol. 1997 Apr;90(2):340-8. (PMID: 9145031) Proc Natl Acad Sci U S A. 2008 Jun 10;105(23):8097-101. (PMID: 18523005) Infect Immun. 1995 Oct;63(10):3790-5. (PMID: 7558281) Cell Host Microbe. 2014 May 14;15(5):578-86. (PMID: 24832452) Genome Res. 2000 Jan;10(1):62-71. (PMID: 10645951) Integr Zool. 2009 Jun;4(2):196-212. (PMID: 21392290) Med Microbiol Immunol. 1993 Nov;182(5):233-42. (PMID: 8283959) Gene. 1996 Dec 5;182(1-2):225-8. (PMID: 8982094) FEMS Microbiol Lett. 2012 Dec;337(2):140-6. (PMID: 23043454) Infect Immun. 2001 Jan;69(1):170-6. (PMID: 11119503) BMC Microbiol. 2012 Dec 13;12:290. (PMID: 23234440) J Enzyme Inhib Med Chem. 2006 Dec;21(6):697-701. (PMID: 17252942) Infect Immun. 1988 Oct;56(10):2749-52. (PMID: 2843471) J Infect Dis. 2004 Aug 15;190(4):783-92. (PMID: 15272407) Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5526-30. (PMID: 16567636) J Infect Dis. 2005 Jun 1;191(11):1907-12. (PMID: 15871125) Cell Microbiol. 2007 Nov;9(11):2658-66. (PMID: 17587333) J Bacteriol. 2008 Dec;190(24):8163-70. (PMID: 18931111) Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14043-8. (PMID: 10570195) Clin Microbiol Rev. 1997 Jan;10(1):35-66. (PMID: 8993858) J Bacteriol. 1945 May;49(5):437-44. (PMID: 16560936) J Bacteriol. 1992 Jul;174(13):4324-30. (PMID: 1624427) Ann Inst Pasteur (Paris). 1964 Sep;107:424-9. (PMID: 14190399) Science. 1996 Jul 19;273(5273):367-70. (PMID: 8662526) J Infect Dis. 1998 Nov;178(5):1406-15. (PMID: 9780262) PLoS One. 2012;7(4):e35598. (PMID: 22530057) Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17837-42. (PMID: 15598742) Eur J Biochem. 2004 Apr;271(7):1357-63. (PMID: 15030486) J Bacteriol. 1946 Oct;52(4):461-6. (PMID: 16561200) J Proteome Res. 2010 Dec 3;9(12):6135-47. (PMID: 20932056) Phytochemistry. 2008 Jan;69(1):18-28. (PMID: 17706733) |
| Grant Information: | Z01 AI000796 United States ImNIH Intramural NIH HHS |
| Contributed Indexing: | Keywords: Yersinia urease; arthropod-borne transmission; evolution; plague; pseudogene |
| Substance Nomenclature: | 0 (Bacterial Proteins) 0 (UreD protein, Bacteria) EC 3.5.1.5 (Urease) |
| Entry Date(s): | Date Created: 20141203 Date Completed: 20150422 Latest Revision: 20250529 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC4284590 |
| DOI: | 10.1073/pnas.1413209111 |
| PMID: | 25453069 |
| Βάση Δεδομένων: | MEDLINE |
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| Items | – Name: Title Label: Title Group: Ti Data: Silencing urease: a key evolutionary step that facilitated the adaptation of Yersinia pestis to the flea-borne transmission route. – Name: Author Label: Authors Group: Au Data: <searchLink fieldCode="AU" term="%22Chouikha+I%22">Chouikha I</searchLink>; Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840 iman.chouikha@nih.gov.<br /><searchLink fieldCode="AU" term="%22Hinnebusch+BJ%22">Hinnebusch BJ</searchLink>; Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840. – Name: TitleSource Label: Source Group: Src Data: <searchLink fieldCode="JN" term="%227505876%22">Proceedings of the National Academy of Sciences of the United States of America</searchLink> [Proc Natl Acad Sci U S A] 2014 Dec 30; Vol. 111 (52), pp. 18709-14. <i>Date of Electronic Publication: </i>2014 Dec 01. – Name: TypePub Label: Publication Type Group: TypPub Data: Journal Article; Research Support, N.I.H., Intramural – Name: Language Label: Language Group: Lang Data: English – Name: TitleSource Label: Journal Info Group: Src Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22National+Academy+of+Sciences%22">National Academy of Sciences </searchLink><i>Country of Publication: </i>United States <i>NLM ID: </i>7505876 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>1091-6490 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2200278424%22">00278424 </searchLink><i>NLM ISO Abbreviation: </i>Proc Natl Acad Sci U S A <i>Subsets: </i>MEDLINE – Name: PublisherInfo Label: Imprint Name(s) Group: PubInfo Data: <i>Original Publication</i>: Washington, DC : National Academy of Sciences – Name: SubjectMESH Label: MeSH Terms Group: Su Data: <searchLink fieldCode="MM" term="%22Bacterial+Proteins%22">Bacterial Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Bacterial+Proteins+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacterial+Proteins%22">Bacterial Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Bacterial+Proteins+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Urease%22">Urease*</searchLink>/<searchLink fieldCode="MM" term="%22Urease+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Urease%22">Urease*</searchLink>/<searchLink fieldCode="MM" term="%22Urease+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Yersinia+pestis%22">Yersinia pestis*</searchLink>/<searchLink fieldCode="MM" term="%22Yersinia+pestis+enzymology%22">enzymology</searchLink> <br /><searchLink fieldCode="MM" term="%22Yersinia+pestis%22">Yersinia pestis*</searchLink>/<searchLink fieldCode="MM" term="%22Yersinia+pestis+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Yersinia+pestis%22">Yersinia pestis*</searchLink>/<searchLink fieldCode="MM" term="%22Yersinia+pestis+pathogenicity%22">pathogenicity</searchLink> <br /><searchLink fieldCode="MM" term="%22Evolution%2C+Molecular%22">Evolution, Molecular*</searchLink> <br /><searchLink fieldCode="MM" term="%22Gene+Silencing%22">Gene Silencing*</searchLink><br /><searchLink fieldCode="MM" term="%22Insect+Vectors%22">Insect Vectors</searchLink>/<searchLink fieldCode="MM" term="%22Insect+Vectors+microbiology%22">*microbiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Xenopsylla%22">Xenopsylla</searchLink>/<searchLink fieldCode="MM" term="%22Xenopsylla+microbiology%22">*microbiology</searchLink><br /><searchLink fieldCode="MH" term="%22Plague%22">Plague</searchLink>/<searchLink fieldCode="MH" term="%22Plague+enzymology%22">enzymology</searchLink> ; <searchLink fieldCode="MH" term="%22Plague%22">Plague</searchLink>/<searchLink fieldCode="MH" term="%22Plague+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Plague%22">Plague</searchLink>/<searchLink fieldCode="MH" term="%22Plague+pathology%22">pathology</searchLink> ; <searchLink fieldCode="MH" term="%22Plague%22">Plague</searchLink>/<searchLink fieldCode="MH" term="%22Plague+transmission%22">transmission</searchLink> ; <searchLink fieldCode="MH" term="%22Yersinia+pseudotuberculosis%22">Yersinia pseudotuberculosis</searchLink>/<searchLink fieldCode="MH" term="%22Yersinia+pseudotuberculosis+enzymology%22">enzymology</searchLink> ; <searchLink fieldCode="MH" term="%22Yersinia+pseudotuberculosis%22">Yersinia pseudotuberculosis</searchLink>/<searchLink fieldCode="MH" term="%22Yersinia+pseudotuberculosis+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Yersinia+pseudotuberculosis%22">Yersinia pseudotuberculosis</searchLink>/<searchLink fieldCode="MH" term="%22Yersinia+pseudotuberculosis+pathogenicity%22">pathogenicity</searchLink> ; <searchLink fieldCode="MH" term="%22Animals%22">Animals</searchLink> ; <searchLink fieldCode="MH" term="%22Humans%22">Humans</searchLink> ; <searchLink fieldCode="MH" term="%22Mutation%22">Mutation</searchLink> – Name: Abstract Label: Abstract Group: Ab Data: The arthropod-borne transmission route of Yersinia pestis, the bacterial agent of plague, is a recent evolutionary adaptation. Yersinia pseudotuberculosis, the closely related food-and water-borne enteric species from which Y. pestis diverged less than 6,400 y ago, exhibits significant oral toxicity to the flea vectors of plague, whereas Y. pestis does not. In this study, we identify the Yersinia urease enzyme as the responsible oral toxin. All Y. pestis strains, including those phylogenetically closest to the Y. pseudotuberculosis progenitor, contain a mutated ureD allele that eliminated urease activity. Restoration of a functional ureD was sufficient to make Y. pestis orally toxic to fleas. Conversely, deletion of the urease operon in Y. pseudotuberculosis rendered it nontoxic. Enzymatic activity was required for toxicity. Because urease-related mortality eliminates 30-40% of infective flea vectors, ureD mutation early in the evolution of Y. pestis was likely subject to strong positive selection because it significantly increased transmission potential. – Name: Comment Label: Comments Group: Commnt Data: Comment in: Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18409-10. doi: 10.1073/pnas.1421887112.. (PMID: <searchLink fieldCode="PM" term="%2225535337%22">25535337)</searchLink> – Name: Ref Label: References Group: RefInfo Data: Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13826-31. (PMID: <searchLink fieldCode="PM" term="%2215358858%22">15358858)</searchLink><br />J Hyg (Lond). 1914 Jan;13(Suppl):423-39. (PMID: <searchLink fieldCode="PM" term="%2220474555%22">20474555)</searchLink><br />Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):577-82. (PMID: <searchLink fieldCode="PM" term="%2223271803%22">23271803)</searchLink><br />Arch Insect Biochem Physiol. 2000 Aug;44(4):162-71. (PMID: <searchLink fieldCode="PM" term="%2210918311%22">10918311)</searchLink><br />Infect Immun. 1997 May;65(5):1985-90. (PMID: <searchLink fieldCode="PM" term="%229125594%22">9125594)</searchLink><br />Infect Immun. 2007 Feb;75(2):774-80. (PMID: <searchLink fieldCode="PM" term="%2217101645%22">17101645)</searchLink><br />Science. 2002 Apr 26;296(5568):733-5. (PMID: <searchLink fieldCode="PM" term="%2211976454%22">11976454)</searchLink><br />Eur J Clin Microbiol Infect Dis. 1999 Jan;18(1):1-15. (PMID: <searchLink fieldCode="PM" term="%2210192708%22">10192708)</searchLink><br />Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6236-41. (PMID: <searchLink fieldCode="PM" term="%2216603630%22">16603630)</searchLink><br />Metallomics. 2009;1(3):207-21. (PMID: <searchLink fieldCode="PM" term="%2220046957%22">20046957)</searchLink><br />J Biol Chem. 2013 May 10;288(19):13178-85. (PMID: <searchLink fieldCode="PM" term="%2223539618%22">23539618)</searchLink><br />J Econ Entomol. 1997 Apr;90(2):340-8. (PMID: <searchLink fieldCode="PM" term="%229145031%22">9145031)</searchLink><br />Proc Natl Acad Sci U S A. 2008 Jun 10;105(23):8097-101. (PMID: <searchLink fieldCode="PM" term="%2218523005%22">18523005)</searchLink><br />Infect Immun. 1995 Oct;63(10):3790-5. (PMID: <searchLink fieldCode="PM" term="%227558281%22">7558281)</searchLink><br />Cell Host Microbe. 2014 May 14;15(5):578-86. (PMID: <searchLink fieldCode="PM" term="%2224832452%22">24832452)</searchLink><br />Genome Res. 2000 Jan;10(1):62-71. (PMID: <searchLink fieldCode="PM" term="%2210645951%22">10645951)</searchLink><br />Integr Zool. 2009 Jun;4(2):196-212. (PMID: <searchLink fieldCode="PM" term="%2221392290%22">21392290)</searchLink><br />Med Microbiol Immunol. 1993 Nov;182(5):233-42. (PMID: <searchLink fieldCode="PM" term="%228283959%22">8283959)</searchLink><br />Gene. 1996 Dec 5;182(1-2):225-8. (PMID: <searchLink fieldCode="PM" term="%228982094%22">8982094)</searchLink><br />FEMS Microbiol Lett. 2012 Dec;337(2):140-6. (PMID: <searchLink fieldCode="PM" term="%2223043454%22">23043454)</searchLink><br />Infect Immun. 2001 Jan;69(1):170-6. (PMID: <searchLink fieldCode="PM" term="%2211119503%22">11119503)</searchLink><br />BMC Microbiol. 2012 Dec 13;12:290. (PMID: <searchLink fieldCode="PM" term="%2223234440%22">23234440)</searchLink><br />J Enzyme Inhib Med Chem. 2006 Dec;21(6):697-701. (PMID: <searchLink fieldCode="PM" term="%2217252942%22">17252942)</searchLink><br />Infect Immun. 1988 Oct;56(10):2749-52. (PMID: <searchLink fieldCode="PM" term="%222843471%22">2843471)</searchLink><br />J Infect Dis. 2004 Aug 15;190(4):783-92. (PMID: <searchLink fieldCode="PM" term="%2215272407%22">15272407)</searchLink><br />Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5526-30. (PMID: <searchLink fieldCode="PM" term="%2216567636%22">16567636)</searchLink><br />J Infect Dis. 2005 Jun 1;191(11):1907-12. (PMID: <searchLink fieldCode="PM" term="%2215871125%22">15871125)</searchLink><br />Cell Microbiol. 2007 Nov;9(11):2658-66. (PMID: <searchLink fieldCode="PM" term="%2217587333%22">17587333)</searchLink><br />J Bacteriol. 2008 Dec;190(24):8163-70. (PMID: <searchLink fieldCode="PM" term="%2218931111%22">18931111)</searchLink><br />Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14043-8. (PMID: <searchLink fieldCode="PM" term="%2210570195%22">10570195)</searchLink><br />Clin Microbiol Rev. 1997 Jan;10(1):35-66. (PMID: <searchLink fieldCode="PM" term="%228993858%22">8993858)</searchLink><br />J Bacteriol. 1945 May;49(5):437-44. (PMID: <searchLink fieldCode="PM" term="%2216560936%22">16560936)</searchLink><br />J Bacteriol. 1992 Jul;174(13):4324-30. (PMID: <searchLink fieldCode="PM" term="%221624427%22">1624427)</searchLink><br />Ann Inst Pasteur (Paris). 1964 Sep;107:424-9. (PMID: <searchLink fieldCode="PM" term="%2214190399%22">14190399)</searchLink><br />Science. 1996 Jul 19;273(5273):367-70. (PMID: <searchLink fieldCode="PM" term="%228662526%22">8662526)</searchLink><br />J Infect Dis. 1998 Nov;178(5):1406-15. (PMID: <searchLink fieldCode="PM" term="%229780262%22">9780262)</searchLink><br />PLoS One. 2012;7(4):e35598. (PMID: <searchLink fieldCode="PM" term="%2222530057%22">22530057)</searchLink><br />Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17837-42. (PMID: <searchLink fieldCode="PM" term="%2215598742%22">15598742)</searchLink><br />Eur J Biochem. 2004 Apr;271(7):1357-63. (PMID: <searchLink fieldCode="PM" term="%2215030486%22">15030486)</searchLink><br />J Bacteriol. 1946 Oct;52(4):461-6. (PMID: <searchLink fieldCode="PM" term="%2216561200%22">16561200)</searchLink><br />J Proteome Res. 2010 Dec 3;9(12):6135-47. (PMID: <searchLink fieldCode="PM" term="%2220932056%22">20932056)</searchLink><br />Phytochemistry. 2008 Jan;69(1):18-28. (PMID: <searchLink fieldCode="PM" term="%2217706733%22">17706733)</searchLink> – Name: GrantInfo Label: Grant Information Group: Grant Data: Z01 AI000796 United States ImNIH Intramural NIH HHS – Name: SubjectMinor Label: Contributed Indexing Group: Data: <i>Keywords: </i>Yersinia urease; arthropod-borne transmission; evolution; plague; pseudogene – Name: NumberCAS Label: Substance Nomenclature Group: ID Data: 0 (Bacterial Proteins)<br />0 (UreD protein, Bacteria)<br />EC 3.5.1.5 (Urease) – Name: DateEntry Label: Entry Date(s) Group: Date Data: <i>Date Created: </i>20141203 <i>Date Completed: </i>20150422 <i>Latest Revision: </i>20250529 – Name: DateUpdate Label: Update Code Group: Date Data: 20260130 – Name: PubmedCentralID Label: PubMed Central ID Group: ID Data: PMC4284590 – Name: DOI Label: DOI Group: ID Data: 10.1073/pnas.1413209111 – Name: AN Label: PMID Group: ID Data: 25453069 |
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| RecordInfo | BibRecord: BibEntity: Identifiers: – Type: doi Value: 10.1073/pnas.1413209111 Languages: – Code: eng Text: English PhysicalDescription: Pagination: StartPage: 18709 Subjects: – SubjectFull: Plague enzymology Type: general – SubjectFull: Plague genetics Type: general – SubjectFull: Plague pathology Type: general – SubjectFull: Plague transmission Type: general – SubjectFull: Yersinia pseudotuberculosis enzymology Type: general – SubjectFull: Yersinia pseudotuberculosis genetics Type: general – SubjectFull: Yersinia pseudotuberculosis pathogenicity Type: general – SubjectFull: Animals Type: general – SubjectFull: Humans Type: general – SubjectFull: Mutation Type: general – SubjectFull: Bacterial Proteins genetics Type: general – SubjectFull: Bacterial Proteins metabolism Type: general – SubjectFull: Urease genetics Type: general – SubjectFull: Urease metabolism Type: general – SubjectFull: Yersinia pestis enzymology Type: general – SubjectFull: Yersinia pestis genetics Type: general – SubjectFull: Yersinia pestis pathogenicity Type: general – SubjectFull: Evolution, Molecular Type: general – SubjectFull: Gene Silencing Type: general – SubjectFull: Insect Vectors microbiology Type: general – SubjectFull: Xenopsylla microbiology Type: general Titles: – TitleFull: Silencing urease: a key evolutionary step that facilitated the adaptation of Yersinia pestis to the flea-borne transmission route. Type: main BibRelationships: HasContributorRelationships: – PersonEntity: Name: NameFull: Chouikha I – PersonEntity: Name: NameFull: Hinnebusch BJ IsPartOfRelationships: – BibEntity: Dates: – D: 30 M: 12 Text: 2014 Dec 30 Type: published Y: 2014 Identifiers: – Type: issn-electronic Value: 1091-6490 Numbering: – Type: volume Value: 111 – Type: issue Value: 52 Titles: – TitleFull: Proceedings of the National Academy of Sciences of the United States of America Type: main |
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