Nutrient depletion may trigger the Yersinia pestis OmpR-EnvZ regulatory system to promote flea-borne plague transmission.
Animals
Bacterial Outer Membrane Proteins
/ genetics
Bacterial Proteins
/ genetics
Biofilms
/ growth & development
Enzyme Activation
/ genetics
Nutrients
/ deficiency
Plague
/ microbiology
Porins
/ genetics
Siphonaptera
/ microbiology
Stomach
/ microbiology
Trans-Activators
/ genetics
Yersinia pestis
/ genetics
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
accepted:
15
08
2019
pubmed:
20
8
2019
medline:
31
3
2020
entrez:
20
8
2019
Statut:
ppublish
Résumé
The flea's lumen gut is a poorly documented environment where the agent of flea-borne plague, Yersinia pestis, must replicate to produce a transmissible infection. Here, we report that both the acidic pH and osmolarity of the lumen's contents display simple harmonic oscillations with different periods. Since an acidic pH and osmolarity are two of three known stimuli of the OmpR-EnvZ two-component system in bacteria, we investigated the role and function of this Y. pestis system in fleas. By monitoring the in vivo expression pattern of three OmpR-EnvZ-regulated genes, we concluded that the flea gut environment triggers OmpR-EnvZ. This activation was not, however, correlated with changes in pH and osmolarity but matched the pattern of nutrient depletion (the third known stimulus for OmpR-EnvZ). Lastly, we found that the OmpR-EnvZ and the OmpF porin are needed to produce the biofilm that ultimately obstructs the flea's gut and thus hastens the flea-borne transmission of plague. Taken as a whole, our data suggest that the flea gut is a complex, fluctuating environment in which Y. pestis senses nutrient depletion via OmpR-EnvZ. Once activated, the latter triggers a molecular program (including at least OmpF) that produces the biofilm required for efficient plague transmission.
Identifiants
pubmed: 31424585
doi: 10.1111/mmi.14372
pmc: PMC6842400
mid: NIHMS1046876
doi:
Substances chimiques
Bacterial Outer Membrane Proteins
0
Bacterial Proteins
0
OmpF protein
0
Porins
0
Trans-Activators
0
osmolarity response regulator proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1471-1482Subventions
Organisme : Intramural NIH HHS
ID : ZIA AI000905-17
Pays : United States
Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Adv Exp Med Biol. 2007;603:192-200
pubmed: 17966415
BMC Microbiol. 2011 Feb 23;11:39
pubmed: 21345178
J Bacteriol. 2018 Apr 9;200(9):
pubmed: 29440252
Can J Microbiol. 2011 Jun;57(6):468-75
pubmed: 21627465
Infect Immun. 2015 Sep;83(9):3638-47
pubmed: 26150539
Nature. 1992 Aug 27;358(6389):727-33
pubmed: 1380671
Structure. 2012 Jul 3;20(7):1154-66
pubmed: 22658749
PLoS One. 2011 Apr 29;6(4):e19267
pubmed: 21559445
J Exp Biol. 1950 Dec;27(3-4):407-19
pubmed: 14803622
J Bacteriol. 2012 Apr;194(8):2036-40
pubmed: 22328669
Front Microbiol. 2018 Feb 27;9:348
pubmed: 29535702
Sci Rep. 2019 Feb 21;9(1):2501
pubmed: 30792499
Microbiology. 2015 Jun;161(6):1198-1210
pubmed: 25804213
J Med Entomol. 2012 Mar;49(2):364-70
pubmed: 22493856
J Hyg (Lond). 1914 Jan;13(Suppl):423-39
pubmed: 20474555
Infect Immun. 2001 Jan;69(1):170-6
pubmed: 11119503
Annu Rev Entomol. 2012;57:61-82
pubmed: 21888520
PLoS One. 2015 Sep 08;10(9):e0137508
pubmed: 26348850
Curr Issues Mol Biol. 2005 Jul;7(2):151-77
pubmed: 16053248
J Bacteriol. 2013 May;195(9):1920-30
pubmed: 23435973
Mol Cell. 2007 Apr 27;26(2):165-74
pubmed: 17466620
J Biol Chem. 1997 Jan 17;272(3):1440-3
pubmed: 8999810
J Exp Biol. 2011 May 1;214(Pt 9):1411-8
pubmed: 21490249
J Bacteriol. 1988 Nov;170(11):5080-5
pubmed: 2846509
Ann Parasitol Hum Comp. 1983;58(5):493-514
pubmed: 6660797
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Microbiology. 2009 Aug;155(Pt 8):2522-31
pubmed: 19443542
Parazitologiia. 1976 Nov-Dec;10(6):544-9
pubmed: 1023147
PLoS Pathog. 2014 Mar 27;10(3):e1004029
pubmed: 24675805
Microbiol Mol Biol Rev. 2003 Dec;67(4):593-656
pubmed: 14665678
J Med Entomol. 1993 Jan;30(1):214-6
pubmed: 8094460
Biochem Biophys Res Commun. 1978 Jul 28;83(2):550-7
pubmed: 358984
J Biol Chem. 1994 Feb 11;269(6):3905-8
pubmed: 7508433
Nat Commun. 2017 Nov 14;8(1):1587
pubmed: 29138484
J Antimicrob Chemother. 1993 Aug;32(2):195-213
pubmed: 8226422
J Bacteriol. 2014 Mar;196(6):1165-73
pubmed: 24391055
J Infect Dis. 2004 Aug 15;190(4):783-92
pubmed: 15272407
Nucleic Acids Res. 2001 May 1;29(9):e45
pubmed: 11328886
Parasitology. 2000 Jun;120 ( Pt 6):547-51
pubmed: 10874717
J Bacteriol. 1990 Feb;172(2):771-8
pubmed: 2404956
Nat Methods. 2005 Jun;2(6):443-8
pubmed: 15908923
Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18709-14
pubmed: 25453069
PLoS Pathog. 2010 Feb 26;6(2):e1000783
pubmed: 20195507
FEMS Microbiol Lett. 2011 Aug;321(1):43-9
pubmed: 21575043
Mol Microbiol. 1996 Jun;20(5):911-7
pubmed: 8809744
Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14043-8
pubmed: 10570195
Cell. 1996 Jan 12;84(1):165-74
pubmed: 8548821
J Mol Biol. 1981 Sep 5;151(1):1-15
pubmed: 6799653
FEMS Microbiol Lett. 2009 Jan;290(1):85-90
pubmed: 19025559
Biotechnol Bioeng. 2011 Mar;108(3):666-75
pubmed: 21246512
J Exp Biol. 2017 Sep 15;220(Pt 18):3355-3362
pubmed: 28931720
J Bacteriol. 1998 Aug;180(15):3917-22
pubmed: 9683489
Environ Microbiol. 2015 Apr;17(4):947-59
pubmed: 25586342
Science. 1996 Jul 19;273(5273):367-70
pubmed: 8662526
Curr Opin Microbiol. 2012 Apr;15(2):118-24
pubmed: 22172627
Mol Microbiol. 2000 Sep;37(6):1470-9
pubmed: 10998177
J Infect Dis. 2014 Nov 1;210(9):1367-75
pubmed: 24813471
Front Microbiol. 2018 Nov 22;9:2656
pubmed: 30524381
Annu Rev Microbiol. 2010;64:539-59
pubmed: 20825354
PLoS Pathog. 2016 Aug 15;12(8):e1005791
pubmed: 27525653
Proc Natl Acad Sci U S A. 2017 Dec 12;114(50):E10792-E10798
pubmed: 29183977
Antimicrob Agents Chemother. 1985 Jan;27(1):84-92
pubmed: 2580479
Science. 2002 Apr 26;296(5568):733-5
pubmed: 11976454
Mol Microbiol. 1990 Jul;4(7):1077-82
pubmed: 1700256
BMC Microbiol. 2011 Feb 23;11:40
pubmed: 21345179
Cell. 2005 Aug 12;122(3):461-72
pubmed: 16096064
Infect Immun. 2000 Jun;68(6):3419-25
pubmed: 10816493
Front Microbiol. 2015 Aug 21;6:862
pubmed: 26347736