title: Species co-occurrence patterns among Lyme borreliosis pathogens in the tick vector Ixodes ricinus.
abstract: Mixed infections have important consequences for the ecology and evolution of host-parasite interactions. In vector-borne diseases, interactions between pathogens occur in both the vertebrate host and the arthropod vector. Spirochete bacteria belonging to the Borrelia burgdorferi sensu lato genospecies complex are transmitted by Ixodes ticks and cause Lyme borreliosis in humans. In Europe, there is a high diversity of Borrelia pathogens, and the main tick vector, Ixodes ricinus, is often infected with multiple Borrelia genospecies. In the present study, we characterized the pairwise interactions between five B. burgdorferi sensu lato genospecies in a large data set of I. ricinus ticks collected from the same field site in Switzerland. We measured two types of pairwise interactions: (i) co-occurrence, whether double infections occurred more or less often than expected, and (ii) spirochete load additivity, whether the total spirochete load in double infections was greater or less than the sum of the single infections. Mixed infections of Borrelia genospecies specialized on different vertebrate reservoir hosts occurred less frequently than expected (negative co-occurrence) and had joint spirochete loads that were lower than the additive expectation (inhibition). In contrast, mixed infections of genospecies that share the same reservoir hosts were more common than expected (positive co-occurrence) and had joint spirochete loads that were similar to or greater than the additive expectation (facilitation). Our study suggests that the vertebrate host plays an important role in structuring the community of B. burgdorferi sensu lato genospecies inside the tick vector.
authors.affiliation: Institute of Biology, Laboratory of Eco-Epidemiology of Parasites, University of Neuchâtel, Neuchâtel, Switzerland.
authors.forename: Coralie
authors.initials: C
authors.lastname: Herrmann
authors.forename: Lise
authors.initials: L
authors.lastname: Gern
authors.forename: Maarten J
authors.initials: MJ
authors.lastname: Voordouw
mesh_terms: D000818:Animals; D058491:Bacterial Load; D015748:Borrelia burgdorferi Group / Q000145:classification* / Q000302:isolation & purification*; D060085:Coinfection / Q000382:microbiology*; D018884:Ixodes / Q000382:microbiology*; D013557:Switzerland
references.citation: Parasitology. 1999 Jan;118 ( Pt 1):33-42
references.pmid: 10070659
references.citation: Appl Environ Microbiol. 2005 Nov;71(11):7203-16
references.pmid: 16269760
references.citation: Proc Natl Acad Sci U S A. 2005 May 24;102(21):7624-8
references.pmid: 15894623
references.citation: Evolution. 2008 Jul;62(7):1700-11
references.pmid: 18384658
references.citation: Appl Environ Microbiol. 2011 Aug 15;77(16):5716-21
references.pmid: 21705536
references.citation: Clin Microbiol Infect. 2001 Sep;7(9):461-9
references.pmid: 11678928
references.citation: J Infect Dis. 2010 Oct 15;202(8):1287-95
references.pmid: 20822454
references.citation: Int J Parasitol. 2013 May;43(6):477-83
references.pmid: 23416154
references.citation: Infect Immun. 1998 Mar;66(3):1248-51
references.pmid: 9488421
references.citation: Evolution. 2006 Jul;60(7):1358-71
references.pmid: 16929653
references.citation: J Med Entomol. 2007 Sep;44(5):869-80
references.pmid: 17915521
references.citation: Q Rev Biol. 1996 Mar;71(1):37-78
references.pmid: 8919665
references.citation: Vector Borne Zoonotic Dis. 2001 Spring;1(1):21-34
references.pmid: 12653133
references.citation: J Med Entomol. 2010 Nov;47(6):1196-204
references.pmid: 21175072
references.citation: J Clin Microbiol. 2002 Jan;40(1):36-43
references.pmid: 11773090
references.citation: Int J Tuberc Lung Dis. 2005 Jun;9(6):592-602
references.pmid: 15971385
references.citation: Proc Biol Sci. 1995 Aug 22;261(1361):209-15
references.pmid: 7568274
references.citation: Appl Environ Microbiol. 2009 Aug;75(16):5410-6
references.pmid: 19542332
references.citation: Science. 2010 Oct 8;330(6001):243-6
references.pmid: 20929776
references.citation: J Parasitol. 2002 Feb;88(1):55-8
references.pmid: 12053980
references.citation: J Clin Microbiol. 2001 Jun;39(6):2237-42
references.pmid: 11376063
references.citation: Acta Trop. 1998 Jun;69(3):213-27
references.pmid: 9638274
references.citation: J Med Entomol. 1996 Jan;33(1):189-92
references.pmid: 8906929
references.citation: Vector Borne Zoonotic Dis. 2010 Oct;10(8):723-30
references.pmid: 20020814
references.citation: J Clin Microbiol. 2002 Dec;40(12):4735-7
references.pmid: 12454181
references.citation: Proc Biol Sci. 2010 Dec 22;277(1701):3693-702
references.pmid: 20667874
references.citation: Parasitology. 2004;129 Suppl:S191-220
references.pmid: 15938512
references.citation: Science. 2001 May 11;292(5519):1099-102
references.pmid: 11352063
references.citation: Proc Biol Sci. 1994 Jan 22;255(1342):81-9
references.pmid: 8153140
references.citation: J Bacteriol. 2011 Mar;193(6):1489-90
references.pmid: 21217002
references.citation: Int J Med Microbiol. 2003 Dec;293(6):421-6
references.pmid: 14760973
references.citation: Zentralbl Bakteriol. 1998 May;287(4):521-38
references.pmid: 9638881
references.citation: Curr HIV Res. 2008 Nov;6(6):485-99
references.pmid: 18991614
references.citation: Ticks Tick Borne Dis. 2010 Mar;1(1):23-9
references.pmid: 21771508
references.citation: Am J Trop Med Hyg. 1990 Apr;42(4):352-7
references.pmid: 2331043
references.citation: Appl Environ Microbiol. 2001 Oct;67(10):4926-9
references.pmid: 11571205
references.citation: Ticks Tick Borne Dis. 2013 Sep;4(5):445-51
references.pmid: 23850119
references.citation: J Med Entomol. 2007 Nov;44(6):1109-17
references.pmid: 18047213
references.citation: Parasitology. 2012 Mar;139(3):330-7
references.pmid: 22217387
references.citation: Trends Microbiol. 2002 Feb;10(2):74-9
references.pmid: 11827808
references.citation: Cell. 2009 Dec 24;139(7):1268-78
references.pmid: 20064373
references.citation: Exp Appl Acarol. 1987 Mar;3(1):53-9
references.pmid: 3134173
references.citation: Infect Immun. 2011 Apr;79(4):1407-17
references.pmid: 21245275
references.citation: Int J Parasitol. 1998 Mar;28(3):377-93
references.pmid: 9559357
references.citation: Ticks Tick Borne Dis. 2011 Dec;2(4):179-82
references.pmid: 22108009
references.citation: Folia Parasitol (Praha). 2004 Mar;51(1):67-71
references.pmid: 15139380
references.citation: J Med Entomol. 1995 Jul;32(4):433-8
references.pmid: 7650703
references.citation: Mol Ecol. 2008 Oct;17(19):4371-81
references.pmid: 19378409
references.citation: Ticks Tick Borne Dis. 2013 Feb;4(1-2):46-51
references.pmid: 23238242
references.citation: Appl Environ Microbiol. 1998 Apr;64(4):1169-74
references.pmid: 9546150