Tick microbial associations at the crossroad of horizontal and vertical transmission pathways.
Anaplasmosis
Ixodes ricinus
Lyme borreliosis
Microbiome
Tick-borne diseases
Transmission dynamics
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
21 Oct 2022
21 Oct 2022
Historique:
received:
29
07
2022
accepted:
29
09
2022
entrez:
22
10
2022
pubmed:
23
10
2022
medline:
26
10
2022
Statut:
epublish
Résumé
Microbial communities can affect disease risk by interfering with the transmission or maintenance of pathogens in blood-feeding arthropods. Here, we investigated whether bacterial communities vary between Ixodes ricinus nymphs which were or were not infected with horizontally transmitted human pathogens. Ticks from eight forest sites were tested for the presence of Borrelia burgdorferi sensu lato, Babesia spp., Anaplasma phagocytophilum, and Neoehrlichia mikurensis by quantitative polymerase chain reaction (qPCR), and their microbiomes were determined by 16S rRNA amplicon sequencing. Tick bacterial communities clustered poorly by pathogen infection status but better by geography. As a second approach, we analysed variation in tick microorganism community structure (in terms of species co-infection) across space using hierarchical modelling of species communities. For that, we analysed almost 14,000 nymphs, which were tested for the presence of horizontally transmitted pathogens B. burgdorferi s.l., A. phagocytophilum, and N. mikurensis, and the vertically transmitted tick symbionts Rickettsia helvetica, Rickettsiella spp., Spiroplasma ixodetis, and Candidatus Midichloria mitochondrii. With the exception of Rickettsiella spp., all microorganisms had either significant negative (R. helvetica and A. phagocytophilum) or positive (S. ixodetis, N. mikurensis, and B. burgdorferi s.l.) associations with M. mitochondrii. Two tick symbionts, R. helvetica and S. ixodetis, were negatively associated with each other. As expected, both B. burgdorferi s.l. and N. mikurensis had a significant positive association with each other and a negative association with A. phagocytophilum. Although these few specific associations do not appear to have a large effect on the entire microbiome composition, they can still be relevant for tick-borne pathogen dynamics. Based on our results, we propose that M. mitochondrii alters the propensity of ticks to acquire or maintain horizontally acquired pathogens. The underlying mechanisms for some of these remarkable interactions are discussed herein and merit further investigation. Positive and negative associations between and within horizontally and vertically transmitted symbionts.
Sections du résumé
BACKGROUND
BACKGROUND
Microbial communities can affect disease risk by interfering with the transmission or maintenance of pathogens in blood-feeding arthropods. Here, we investigated whether bacterial communities vary between Ixodes ricinus nymphs which were or were not infected with horizontally transmitted human pathogens.
METHODS
METHODS
Ticks from eight forest sites were tested for the presence of Borrelia burgdorferi sensu lato, Babesia spp., Anaplasma phagocytophilum, and Neoehrlichia mikurensis by quantitative polymerase chain reaction (qPCR), and their microbiomes were determined by 16S rRNA amplicon sequencing. Tick bacterial communities clustered poorly by pathogen infection status but better by geography. As a second approach, we analysed variation in tick microorganism community structure (in terms of species co-infection) across space using hierarchical modelling of species communities. For that, we analysed almost 14,000 nymphs, which were tested for the presence of horizontally transmitted pathogens B. burgdorferi s.l., A. phagocytophilum, and N. mikurensis, and the vertically transmitted tick symbionts Rickettsia helvetica, Rickettsiella spp., Spiroplasma ixodetis, and Candidatus Midichloria mitochondrii.
RESULTS
RESULTS
With the exception of Rickettsiella spp., all microorganisms had either significant negative (R. helvetica and A. phagocytophilum) or positive (S. ixodetis, N. mikurensis, and B. burgdorferi s.l.) associations with M. mitochondrii. Two tick symbionts, R. helvetica and S. ixodetis, were negatively associated with each other. As expected, both B. burgdorferi s.l. and N. mikurensis had a significant positive association with each other and a negative association with A. phagocytophilum. Although these few specific associations do not appear to have a large effect on the entire microbiome composition, they can still be relevant for tick-borne pathogen dynamics.
CONCLUSIONS
CONCLUSIONS
Based on our results, we propose that M. mitochondrii alters the propensity of ticks to acquire or maintain horizontally acquired pathogens. The underlying mechanisms for some of these remarkable interactions are discussed herein and merit further investigation. Positive and negative associations between and within horizontally and vertically transmitted symbionts.
Identifiants
pubmed: 36271430
doi: 10.1186/s13071-022-05519-w
pii: 10.1186/s13071-022-05519-w
pmc: PMC9585727
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
380Informations de copyright
© 2022. The Author(s).
Références
PLoS Negl Trop Dis. 2016 Mar 17;10(3):e0004539
pubmed: 26986203
Ticks Tick Borne Dis. 2014 Oct;5(6):917-23
pubmed: 25108783
Ticks Tick Borne Dis. 2021 Jul;12(4):101707
pubmed: 33813285
Microbiome. 2022 Aug 4;10(1):120
pubmed: 35927748
Parasit Vectors. 2011 Dec 07;4:228
pubmed: 22152674
Parasit Vectors. 2018 Aug 6;11(1):454
pubmed: 30081938
Appl Environ Microbiol. 2003 May;69(5):2825-30
pubmed: 12732554
PLoS One. 2012;7(3):e32942
pubmed: 22412957
Clin Microbiol Infect. 2015 Jul;21(7):631-9
pubmed: 25700888
Environ Microbiol. 2006 Jul;8(7):1280-7
pubmed: 16817936
PLoS One. 2012;7(1):e30692
pubmed: 22292021
Nat Commun. 2017 Aug 4;8(1):184
pubmed: 28775250
Appl Environ Microbiol. 2006 Jul;72(7):4805-10
pubmed: 16820474
Int J Parasitol. 2013 Jul;43(8):603-11
pubmed: 23597868
ISME J. 2017 Mar;11(3):813-816
pubmed: 27858931
ISME J. 2013 Jan;7(1):221-3
pubmed: 22739493
Proc Biol Sci. 2019 Oct 9;286(1912):20191109
pubmed: 31575371
Trends Genet. 2022 Jul;38(7):708-723
pubmed: 35314082
Ticks Tick Borne Dis. 2014 Apr;5(3):245-51
pubmed: 24582511
Nat Commun. 2020 May 4;11(1):2187
pubmed: 32366903
Proc Biol Sci. 2006 May 22;273(1591):1273-80
pubmed: 16720402
ISME J. 2016 Aug;10(8):1846-55
pubmed: 26882265
Parasit Vectors. 2017 Sep 19;10(1):433
pubmed: 28927432
PLoS One. 2011;6(10):e25604
pubmed: 22022422
J Med Entomol. 2002 Nov;39(6):809-13
pubmed: 12495176
Appl Environ Microbiol. 1997 Oct;63(10):3926-32
pubmed: 9327557
Front Biosci. 2008 May 01;13:6938-46
pubmed: 18508706
J Clin Microbiol. 2004 Jul;42(7):3164-8
pubmed: 15243077
Parasit Vectors. 2012 Aug 04;5:156
pubmed: 22862883
Environ Microbiol. 2013 Feb;15(2):663-73
pubmed: 23279105
Front Cell Infect Microbiol. 2013 Jul 30;3:36
pubmed: 23908971
Sci Rep. 2021 Aug 25;11(1):17148
pubmed: 34433845
J Med Entomol. 2008 Mar;45(2):289-97
pubmed: 18402145
Ecol Lett. 2017 May;20(5):561-576
pubmed: 28317296
Mol Ecol. 2017 Jun;26(11):2905-2921
pubmed: 28281305
Exp Appl Acarol. 2016 Mar;68(3):279-97
pubmed: 26081117
Scand J Infect Dis. 2010 Aug;42(8):579-85
pubmed: 20429719
Appl Environ Microbiol. 2006 Dec;72(12):7594-601
pubmed: 17028227
Microbiome. 2021 Jul 3;9(1):153
pubmed: 34217365
Proc Natl Acad Sci U S A. 2017 Jan 31;114(5):E781-E790
pubmed: 28096373
PLoS One. 2011 Feb 28;6(2):e17035
pubmed: 21386965
Parasit Vectors. 2014 Aug 15;7:365
pubmed: 25127547
Vector Borne Zoonotic Dis. 2013 Jul;13(7):438-42
pubmed: 23590321
Immunol Rev. 2017 Sep;279(1):70-89
pubmed: 28856738
Parasit Vectors. 2012 Apr 19;5:74
pubmed: 22515314
J Med Microbiol. 2020 Jun;69(6):781-791
pubmed: 32478654
Methods Ecol Evol. 2020 Mar;11(3):442-447
pubmed: 32194928
Cell Host Microbe. 2011 Oct 20;10(4):307-10
pubmed: 22018231
Front Cell Infect Microbiol. 2018 Sep 03;8:308
pubmed: 30234029
Parasit Vectors. 2015 Dec 18;8:643
pubmed: 26684199
Ticks Tick Borne Dis. 2015 Apr;6(3):297-302
pubmed: 25773931
Parasit Vectors. 2016 Feb 20;9:97
pubmed: 26896940
Ticks Tick Borne Dis. 2019 Aug;10(5):1070-1077
pubmed: 31176662
Parasit Vectors. 2019 Sep 6;12(1):434
pubmed: 31492171
Ticks Tick Borne Dis. 2018 Jan;9(1):18-24
pubmed: 29103949
Appl Environ Microbiol. 2015 Sep;81(18):6200-9
pubmed: 26150449
J Med Entomol. 2004 May;41(3):277-86
pubmed: 15185926
PeerJ. 2019 Dec 19;7:e8217
pubmed: 31875152
Parasitology. 2003 Jan;126(Pt 1):11-20
pubmed: 12613759
Ticks Tick Borne Dis. 2019 Apr;10(3):575-584
pubmed: 30744948
Tissue Cell. 2004 Feb;36(1):43-53
pubmed: 14729452
Emerg Infect Dis. 2020 Feb;26(2):371-374
pubmed: 31961304
Lancet. 2013 Aug 17;382(9892):658
pubmed: 23953389
Ticks Tick Borne Dis. 2014 Oct;5(6):810-7
pubmed: 25113977
Appl Environ Microbiol. 2014 Mar;80(5):1645-9
pubmed: 24375128
Mol Ecol. 2008 Oct;17(19):4371-81
pubmed: 19378409
Trends Parasitol. 2011 Nov;27(11):514-22
pubmed: 21697014
Folia Parasitol (Praha). 1996;43(1):75-9
pubmed: 8682412
Cell. 2020 Dec 10;183(6):1562-1571.e12
pubmed: 33306955
Microbiome. 2018 Aug 13;6(1):141
pubmed: 30103809
Parasit Vectors. 2020 Jan 20;13(1):34
pubmed: 31959217