Coxiella burnetii and Related Tick Endosymbionts Evolved from Pathogenic Ancestors.
Coxiella
endosymbiont
heme
pathogen
tick
Journal
Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707
Informations de publication
Date de publication:
06 07 2021
06 07 2021
Historique:
accepted:
12
05
2021
pubmed:
20
5
2021
medline:
1
4
2022
entrez:
19
5
2021
Statut:
ppublish
Résumé
Both symbiotic and pathogenic bacteria in the family Coxiellaceae cause morbidity and mortality in humans and animals. For instance, Coxiella-like endosymbionts (CLEs) improve the reproductive success of ticks-a major disease vector, while Coxiella burnetii causes human Q fever, and uncharacterized coxiellae infect both animals and humans. To better understand the evolution of pathogenesis and symbiosis in this group of intracellular bacteria, we sequenced the genome of a CLE present in the soft tick Ornithodoros amblus (CLEOA) and compared it to the genomes of other bacteria in the order Legionellales. Our analyses confirmed that CLEOA is more closely related to C. burnetii, the human pathogen, than to CLEs in hard ticks, and showed that most clades of CLEs contain both endosymbionts and pathogens, indicating that several CLE lineages have evolved independently from pathogenic Coxiella. We also determined that the last common ancestorof CLEOA and C. burnetii was equipped to infect macrophages and that even though horizontal gene transfer (HGT) contributed significantly to the evolution of C. burnetii, most acquisition events occurred primarily in ancestors predating the CLEOA-C. burnetii divergence. These discoveries clarify the evolution of C. burnetii, which previously was assumed to have emerged when an avirulent tick endosymbiont recently gained virulence factors via HGT. Finally, we identified several metabolic pathways, including heme biosynthesis, that are likely critical to the intracellular growth of the human pathogen but not the tick symbiont, and show that the use of heme analog is a promising approach to controlling C. burnetii infections.
Identifiants
pubmed: 34009306
pii: 6278299
doi: 10.1093/gbe/evab108
pmc: PMC8290121
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIAID NIH HHS
ID : R03 AI123464
Pays : United States
Organisme : NIAID NIH HHS
ID : R03 AI133023
Pays : United States
Organisme : NIAID NIH HHS
ID : R15 AI126385
Pays : United States
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
Ticks Tick Borne Dis. 2012 Sep;3(4):203-6
pubmed: 22480930
Mol Microbiol. 1999 Nov;34(4):799-809
pubmed: 10564519
Genome Biol Evol. 2015 Jan 23;7(3):831-8
pubmed: 25618142
Annu Rev Microbiol. 2011;65:111-28
pubmed: 21639786
Nat Genet. 2016 Feb;48(2):167-75
pubmed: 26752266
J Bacteriol. 1983 May;154(2):591-7
pubmed: 6302078
Cell. 2002 Mar 8;108(5):583-6
pubmed: 11893328
Sci Rep. 2016 Sep 20;6:33670
pubmed: 27645766
Syst Biol. 2007 Aug;56(4):564-77
pubmed: 17654362
FASEB J. 2007 Apr;21(4):1058-66
pubmed: 17227954
Adv Exp Med Biol. 2012;984:39-63
pubmed: 22711626
J Agric Food Chem. 1999 Jan;47(1):231-6
pubmed: 10563877
Bioinformatics. 2010 Nov 15;26(22):2914-5
pubmed: 20876605
Mol Microbiol. 1999 Jan;31(2):429-42
pubmed: 10027961
Trends Parasitol. 2020 Oct;36(10):816-825
pubmed: 32811753
Methods Mol Biol. 2019;1962:1-14
pubmed: 31020551
Nat Rev Microbiol. 2011 Nov 08;10(1):13-26
pubmed: 22064560
Nat Methods. 2012 Jul 30;9(8):772
pubmed: 22847109
Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21755-60
pubmed: 21098666
Z Parasitenkd. 1972;39(3):201-9
pubmed: 5057359
J Bacteriol. 2014 Jun;196(11):1925-40
pubmed: 24610709
Ticks Tick Borne Dis. 2019 Jun;10(4):798-804
pubmed: 30922601
Environ Microbiol. 2018 May;20(5):1751-1764
pubmed: 29575448
Trends Parasitol. 2017 Aug;33(8):633-644
pubmed: 28549573
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
FEMS Microbiol Lett. 2015 Sep;362(17):fnv132
pubmed: 26269380
Pharmacol Rev. 1998 Dec;50(4):665-82
pubmed: 9860806
Nucleic Acids Res. 1987 Feb 11;15(3):1281-95
pubmed: 3547335
PLoS Pathog. 2019 Dec 23;15(12):e1007855
pubmed: 31869379
PLoS Biol. 2005 May;3(5):e130
pubmed: 15799709
PLoS One. 2016 May 31;11(5):e0156710
pubmed: 27244230
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Front Cell Infect Microbiol. 2017 Jan 26;7:12
pubmed: 28184354
mSphere. 2020 Jul 22;5(4):
pubmed: 32699121
Infect Immun. 2011 Jan;79(1):414-20
pubmed: 21078859
Nat Methods. 2014 Nov;11(11):1144-6
pubmed: 25218180
Bioorg Chem. 2003 Feb;31(1):24-43
pubmed: 12697167
Front Microbiol. 2020 Apr 22;11:493
pubmed: 32390951
Biochem Biophys Res Commun. 1992 Dec 30;189(3):1491-7
pubmed: 1336371
RNA. 2014 Jul;20(7):994-1003
pubmed: 24865611
PLoS Pathog. 2015 May 15;11(5):e1004892
pubmed: 25978383
Vet Pathol. 2008 Mar;45(2):247-54
pubmed: 18424842
Genome Biol Evol. 2010;2:708-18
pubmed: 20829280
PLoS One. 2016 Feb 24;11(2):e0149957
pubmed: 26909555
J Biol Chem. 1990 Oct 5;265(28):17215-21
pubmed: 2211622
Mol Ecol. 2020 Mar;29(5):1016-1029
pubmed: 32034827
Mol Ecol. 2017 Jun;26(11):2905-2921
pubmed: 28281305
J Parasitol. 1980 Apr;66(2):312-23
pubmed: 7391872
Genome Biol Evol. 2015 May 28;7(6):1779-96
pubmed: 26025560
Clin Microbiol Rev. 2017 Jan;30(1):115-190
pubmed: 27856520
Sci Transl Med. 2018 Sep 26;10(460):
pubmed: 30257953
J Bacteriol. 2001 Apr;183(8):2454-62
pubmed: 11274104
Cell Microbiol. 2020 May;22(5):e13154
pubmed: 31872956
Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):769-74
pubmed: 20080750
Emerg Infect Dis. 2016 Feb;22(2):285-8
pubmed: 26811945
Nucleic Acids Res. 2018 Jul 2;46(W1):W200-W204
pubmed: 29905871
J Biol Chem. 2018 Nov 30;293(48):18636-18645
pubmed: 30315113
Genome Res. 2017 May;27(5):824-834
pubmed: 28298430
Appl Environ Microbiol. 2007 Oct;73(20):6584-94
pubmed: 17720830
Genome Biol Evol. 2018 Feb 1;10(2):607-615
pubmed: 29385445
Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10169-76
pubmed: 25713367
Syst Biol. 2012 May;61(3):539-42
pubmed: 22357727
Clin Microbiol Rev. 1999 Oct;12(4):518-53
pubmed: 10515901
Parasit Vectors. 2020 Feb 14;13(1):75
pubmed: 32059686
Infect Immun. 2009 Feb;77(2):642-56
pubmed: 19047403
Exp Appl Acarol. 2017 Dec;73(3-4):429-438
pubmed: 29197022
Antimicrob Agents Chemother. 2015 Dec;59(12):7657-65
pubmed: 26416873
Immunol Rev. 2015 Mar;264(1):249-63
pubmed: 25703564
J Bacteriol. 2019 Oct 21;201(22):
pubmed: 31451541
mBio. 2011 Sep 01;2(4):e00175-11
pubmed: 21862628
Sci Rep. 2017 Dec 14;7(1):17554
pubmed: 29242567
Adv Exp Med Biol. 2012;984:199-213
pubmed: 22711633
Mol Ecol. 2017 Apr;26(8):2199-2203
pubmed: 28419609
J Biol Chem. 2020 May 22;295(21):7391-7403
pubmed: 32303638
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5455-60
pubmed: 12704232
J Bacteriol. 2000 Jul;182(13):3867-9
pubmed: 10851009
Front Cell Infect Microbiol. 2017 May 31;7:190
pubmed: 28620582
J Bacteriol. 2013 Jul;195(14):3269-76
pubmed: 23687269
PLoS One. 2007 May 02;2(5):e405
pubmed: 17476327
Infect Immun. 2020 May 20;88(6):
pubmed: 32205404
Avian Dis. 2008 Sep;52(3):426-32
pubmed: 18939630
Biofactors. 2014 May-Jun;40(3):303-12
pubmed: 24532037
Infect Immun. 2008 Feb;76(2):497-509
pubmed: 18025096
Trends Parasitol. 2015 Nov;31(11):536-552
pubmed: 26458781
ISME J. 2018 Mar;12(3):898-908
pubmed: 29362506
PLoS Pathog. 2014 Mar 20;10(3):e1004013
pubmed: 24651569
BMC Bioinformatics. 2010 Mar 08;11:119
pubmed: 20211023
Front Cell Infect Microbiol. 2018 Sep 10;8:316
pubmed: 30250828
J Bacteriol. 2017 Jun 13;199(13):
pubmed: 28439040
Curr Biol. 2018 Jun 18;28(12):1896-1902.e5
pubmed: 29861133
PLoS One. 2014 Jun 20;9(6):e100147
pubmed: 24949863
Proc Natl Acad Sci U S A. 2012 Sep 4;109(36):14504-7
pubmed: 22908296
J Bacteriol. 2010 Dec;192(23):6154-9
pubmed: 20870767
Am J Trop Med Hyg. 2017 Nov;97(5):1319-1322
pubmed: 28820698
Avian Pathol. 2020 Jun;49(3):268-274
pubmed: 32054295
Front Cell Infect Microbiol. 2017 May 10;7:174
pubmed: 28540258
Nat Biotechnol. 2013 Jun;31(6):533-8
pubmed: 23707974
Nucleic Acids Res. 2003 Apr 15;31(8):2242-51
pubmed: 12682375
Science. 2006 Oct 13;314(5797):267
pubmed: 17038615
BMC Microbiol. 2018 Apr 16;18(1):33
pubmed: 29661138
Tuberculosis (Edinb). 2012 May;92(3):202-10
pubmed: 22361385
Genome Biol. 2015 Aug 06;16:157
pubmed: 26243257
J Mol Evol. 1997 Apr;44(4):383-97
pubmed: 9089078
Biol Direct. 2016 Oct 21;11(1):55
pubmed: 27769290
Nature. 2000 May 18;405(6784):299-304
pubmed: 10830951
Nucleic Acids Res. 2007;35(9):3100-8
pubmed: 17452365
Parasit Vectors. 2018 Apr 13;11(1):242
pubmed: 29653599
PLoS Pathog. 2014 Jul 31;10(7):e1004286
pubmed: 25080348
Biochim Biophys Acta Gene Regul Mech. 2018 Apr;1861(4):419-432
pubmed: 29378328
Lett Appl Microbiol. 2020 Sep;71(3):320-326
pubmed: 32491210