Transcriptomic profiling of the digestive tract of the rat flea, Xenopsylla cheopis, following blood feeding and infection with Yersinia pestis.
Journal
PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
04
02
2020
accepted:
10
08
2020
revised:
30
09
2020
pubmed:
19
9
2020
medline:
3
11
2020
entrez:
18
9
2020
Statut:
epublish
Résumé
Yersinia pestis, the causative agent of plague, is a highly lethal pathogen transmitted by the bite of infected fleas. Once ingested by a flea, Y. pestis establish a replicative niche in the gut and produce a biofilm that promotes foregut colonization and transmission. The rat flea Xenopsylla cheopis is an important vector to several zoonotic bacterial pathogens including Y. pestis. Some fleas naturally clear themselves of infection; however, the physiological and immunological mechanisms by which this occurs are largely uncharacterized. To address this, RNA was extracted, sequenced, and distinct transcript profiles were assembled de novo from X. cheopis digestive tracts isolated from fleas that were either: 1) not fed for 5 days; 2) fed sterile blood; or 3) fed blood containing ~5x108 CFU/ml Y. pestis KIM6+. Analysis and comparison of the transcript profiles resulted in identification of 23 annotated (and 11 unknown or uncharacterized) digestive tract transcripts that comprise the early transcriptional response of the rat flea gut to infection with Y. pestis. The data indicate that production of antimicrobial peptides regulated by the immune-deficiency pathway (IMD) is the primary flea immune response to infection with Y. pestis. The remaining infection-responsive transcripts, not obviously associated with the immune response, were involved in at least one of 3 physiological themes: 1) alterations to chemosensation and gut peristalsis; 2) modification of digestion and metabolism; and 3) production of chitin-binding proteins (peritrophins). Despite producing several peritrophin transcripts shortly after feeding, including a subset that were infection-responsive, no thick peritrophic membrane was detectable by histochemistry or electron microscopy of rat flea guts for the first 24 hours following blood-feeding. Here we discuss the physiological implications of rat flea infection-responsive transcripts, the function of X. cheopis peritrophins, and the mechanisms by which Y. pestis may be cleared from the flea gut.
Identifiants
pubmed: 32946437
doi: 10.1371/journal.pntd.0008688
pii: PNTD-D-20-00176
pmc: PMC7526888
doi:
Types de publication
Journal Article
Research Support, N.I.H., Intramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0008688Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Elife. 2017 Jan 12;6:
pubmed: 28079523
Annu Rev Entomol. 2012;57:61-82
pubmed: 21888520
Insect Biochem Mol Biol. 2006 Apr;36(4):322-35
pubmed: 16551546
Infect Immun. 2017 Dec 19;86(1):
pubmed: 29084898
Science. 1996 Jul 19;273(5273):367-70
pubmed: 8662526
Insect Mol Biol. 2010 Apr;19(2):229-41
pubmed: 20017753
PLoS One. 2015 Jul 15;10(7):e0133318
pubmed: 26177454
BMC Genomics. 2017 Oct 11;18(1):770
pubmed: 29020917
Annu Rev Microbiol. 2017 Sep 8;71:215-232
pubmed: 28886687
PLoS Pathog. 2017 May 17;13(5):e1006391
pubmed: 28545061
Nat Rev Immunol. 2004 Jul;4(7):521-7
pubmed: 15229471
Cell Metab. 2010 Oct 6;12(4):386-397
pubmed: 20889130
Life Sci. 2013 Mar 19;92(8-9):394-403
pubmed: 22877650
Insect Biochem Mol Biol. 2003 Nov;33(11):1061-73
pubmed: 14563358
Bioinformatics. 2007 Nov 1;23(21):2947-8
pubmed: 17846036
Insect Mol Biol. 1999 Feb;8(1):11-22
pubmed: 9927170
Insect Sci. 2019 Jun;26(3):424-440
pubmed: 29064633
Cell Host Microbe. 2014 May 14;15(5):578-86
pubmed: 24832452
Annu Rev Immunol. 2007;25:697-743
pubmed: 17201680
Pest Manag Sci. 2017 Jan;73(1):206-216
pubmed: 27060284
PLoS Pathog. 2018 Jan 22;14(1):e1006859
pubmed: 29357385
Curr Opin Microbiol. 2012 Jun;15(3):239-46
pubmed: 22406208
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10692-7
pubmed: 11535825
Pest Manag Sci. 2003 Oct;59(10):1063-75
pubmed: 14561063
Microbiology (Reading). 1998 Aug;144 ( Pt 8):2179-88
pubmed: 9720039
Annu Rev Entomol. 2010;55:485-504
pubmed: 19743913
Microbiology (Reading). 2015 Jun;161(6):1198-1210
pubmed: 25804213
Mol Microbiol. 2004 Jun;52(5):1363-73
pubmed: 15165239
J Immunol. 2014 Apr 15;192(8):3455-62
pubmed: 24706930
Parasit Vectors. 2015 Jul 14;8:368
pubmed: 26168790
Cell. 2012 Dec 7;151(6):1345-57
pubmed: 23217715
J Med Entomol. 2012 Mar;49(2):364-70
pubmed: 22493856
PLoS One. 2015 Jun 01;10(6):e0128203
pubmed: 26030610
Infect Immun. 2010 Dec;78(12):5086-98
pubmed: 20876291
J Hyg (Lond). 1914 Jan;13(Suppl):423-39
pubmed: 20474555
J Parasitol. 1960 Jun;46:362-72
pubmed: 14425284
Genomics. 2015 Dec;106(6):393-403
pubmed: 26376410
J Biol Chem. 2005 Oct 7;280(40):34048-55
pubmed: 16081424
Curr Biol. 2017 Jan 9;27(1):96-102
pubmed: 27989672
J Biol Chem. 1991 Dec 25;266(36):24520-5
pubmed: 1761552
Curr Biol. 2002 Oct 15;12(20):1728-37
pubmed: 12401167
PLoS One. 2011;6(12):e28525
pubmed: 22216098
Science. 2005 Nov 4;310(5749):847-50
pubmed: 16272120
Cell Signal. 2009 Jun;21(6):836-46
pubmed: 19385042
J Bacteriol. 2013 May;195(9):1920-30
pubmed: 23435973
Proc Natl Acad Sci U S A. 1998 May 12;95(10):5700-5
pubmed: 9576947
Gen Comp Endocrinol. 2015 Sep 15;221:255-66
pubmed: 25616197
mSystems. 2019 Feb 19;4(1):
pubmed: 30801031
Biol Chem. 2016 Sep 1;397(9):939-45
pubmed: 27105487
J Immunol. 2014 Jul 15;193(2):773-82
pubmed: 24913976
Genome Res. 2002 Sep;12(9):1357-69
pubmed: 12213773
Sci Rep. 2015 Jul 08;5:11947
pubmed: 26153094
Am J Trop Med Hyg. 2000 May;62(5):552-60
pubmed: 11289663
EMBO J. 1983;2(4):571-6
pubmed: 6628360
Annu Rev Entomol. 1997;42:525-50
pubmed: 15012322
Cell Host Microbe. 2009 Feb 19;5(2):200-11
pubmed: 19218090
Sci Rep. 2017 May 9;7(1):1619
pubmed: 28487555
J Neurobiol. 2005 May;63(2):146-58
pubmed: 15719418
J Med Entomol. 2015 May;52(3):351-8
pubmed: 26334808
PLoS Pathog. 2020 Apr 15;16(4):e1008440
pubmed: 32294143
J Invertebr Pathol. 2016 Jul;138:10-7
pubmed: 27261060
Dev Comp Immunol. 2019 Sep;98:76-79
pubmed: 31002845
BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Insect Biochem Mol Biol. 2002 May;32(5):517-23
pubmed: 11891128
Biochimie. 2016 Mar;122:255-69
pubmed: 26453810
Microb Pathog. 2011 Dec;51(6):389-95
pubmed: 21964409
J Med Entomol. 1993 Jan;30(1):214-6
pubmed: 8094460
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Mol Biol Evol. 2013 Dec;30(12):2725-9
pubmed: 24132122
Science. 2001 Mar 30;291(5513):2600-2
pubmed: 11283371
Cell Mol Life Sci. 2010 Apr;67(7):1177-88
pubmed: 20049505
Mol Endocrinol. 2007 Oct;21(10):2320-33
pubmed: 17595322
Insect Mol Biol. 2001 Aug;10(4):293-302
pubmed: 11520352
Genetics. 2018 Oct;210(2):357-396
pubmed: 30287514
Proc Natl Acad Sci U S A. 2013 Oct 22;110(43):17504-9
pubmed: 24101462
Dev Comp Immunol. 2007;31(7):647-56
pubmed: 17161866
Nat Rev Microbiol. 2016 Aug 11;14(9):563-75
pubmed: 27510863
J Infect Dis. 2004 Aug 15;190(4):783-92
pubmed: 15272407
Methods Mol Biol. 2019;2010:167-178
pubmed: 31177438
Dev Comp Immunol. 2015 Nov;53(1):134-44
pubmed: 26165161
J Infect Dis. 2005 Jun 1;191(11):1907-12
pubmed: 15871125
Science. 2011 Oct 21;334(6054):362-5
pubmed: 22021855
Microbiology (Reading). 2015 Mar;161(Pt 3):628-38
pubmed: 25533446
Nat Genet. 2003 Oct;35(2):180-4
pubmed: 12958599
Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10343-7
pubmed: 8816802
PLoS Negl Trop Dis. 2016 Feb 01;10(2):e0004413
pubmed: 26829486
PLoS Pathog. 2010 Feb 26;6(2):e1000783
pubmed: 20195507
J Med Entomol. 1992 Mar;29(2):203-6
pubmed: 1495030
Genetics. 2001 Nov;159(3):1059-72
pubmed: 11729153
Nat Rev Immunol. 2014 Dec;14(12):796-810
pubmed: 25421701
Exp Mol Med. 2010 Jan 31;42(1):12-20
pubmed: 19887892
Glycobiology. 2005 Feb;15(2):153-64
pubmed: 15385431
Antimicrob Agents Chemother. 2015 May;59(5):2508-14
pubmed: 25666157
Gen Comp Endocrinol. 2009 May 15;162(1):93-104
pubmed: 18775723
Cell Tissue Res. 2000 Apr;300(1):153-63
pubmed: 10805084
Nature. 1999 Aug 5;400(6744):517-8
pubmed: 10448851
Genome Res. 2009 Jun;19(6):1117-23
pubmed: 19251739
J Mol Diagn. 2012 Jan;14(1):22-9
pubmed: 22166544
J Infect Dis. 2013 May 15;207(10):1535-43
pubmed: 23402825
Trends Neurosci. 2000 Apr;23(4):159-66
pubmed: 10717675
Annu Rev Entomol. 2016;61:177-96
pubmed: 26982439
Science. 2002 Apr 26;296(5568):733-5
pubmed: 11976454