Colonization and pathology of Borrelia afzelii in its natural hosts

Zhong, Xianqiong; Nouri, Meisam; Råberg, Lars

doi:10.1016/j.ttbdis.2019.03.017

Cited by 12 publications

(17 citation statements)

References 53 publications

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“…Previous studies have found that the bacterial load is about ten times higher in B. afzelii-infected bank voles than infected yellow-necked mice, indicating that mice are more resistant (Råberg, 2012;Zhong et al, 2019). The same pattern was found in the present study, despite a relatively small data set.…”

Section: Discussionsupporting

confidence: 89%

“…In humans, untreated Borrelia infection may develop into diverse clinical manifestations, including neuroborreliosis, Lyme arthritis and carditis (Stanek, Wormser, Gray, & Strle, 2012), and at least some strains of laboratory mice display similar symptoms (Lin et al, 2014;Wooten & Weis, 2001). In contrast, no or limited pathology occurs in the natural hosts, like white-footed mouse (Peromyscus leucopus), bank vole (Myodes glareolus), and yellow-necked mouse (Apodemus flavicollis) (Moody, Terwilliger, Hansen, & Barthold, 1994;Zhong, Nouri, & Råberg, 2019). Previous studies have shown that the bacterial load of B. afzelii in infected individuals differs considerably between host species; for example, bank voles have ten times higher loads than yellow-necked mice (Råberg, 2012;Zhong et al, 2019).…”

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confidence: 99%

“…In contrast, no or limited pathology occurs in the natural hosts, like white-footed mouse (Peromyscus leucopus), bank vole (Myodes glareolus), and yellow-necked mouse (Apodemus flavicollis) (Moody, Terwilliger, Hansen, & Barthold, 1994;Zhong, Nouri, & Råberg, 2019). Previous studies have shown that the bacterial load of B. afzelii in infected individuals differs considerably between host species; for example, bank voles have ten times higher loads than yellow-necked mice (Råberg, 2012;Zhong et al, 2019).…”

mentioning

confidence: 99%

“…A strong and effective antibody response against B. burgdorferi infection in mice also occurs (Connolly & Benach, 2005;McKisic & Barthold, 2000). Despite the immune response, bacteria typically disseminate from the tick bite site and colonize internal tissues (Zhong et al, 2019). Studies of both B. burgdorferi and B. afzelii have shown that infections may be chronic (persist for life), although the length of the infection may depend on bacterial strain (Humair, Rais, & Gern, 1999;Kurtenbach et al, 2006).…”

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confidence: 99%

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Comparison of spleen transcriptomes of two wild rodent species reveals differences in the immune response against Borrelia afzelii

Zhong

Lundberg

Råberg

2020

Ecology and Evolution

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Different host species often differ considerably in susceptibility to a given pathogen, but the causes of such differences are rarely known. The natural hosts of the tick‐transmitted bacterium Borrelia afzelii, which is one of causative agents of Lyme borreliosis in humans, include a variety of small mammals like voles and mice. Previous studies have shown that B. afzelii‐infected bank voles (Myodes glareolus) have about ten times higher bacterial load than infected yellow‐necked mice (Apodemus flavicollis), indicating that these two species differ in resistance. In this study, we compared the immune response to B. afzelii infection in these host species by using RNA sequencing to quantify gene expression in spleen. Gene set enrichment analysis (GSEA) showed that several immune pathways were down‐regulated in infected animals in both bank voles and yellow‐necked mice. Moreover, IFNα response was up‐regulated in B. afzelii‐infected yellow‐necked mice, while IL6 signaling and the complement pathway were down‐regulated in infected bank voles; differences in regulation of these three pathways between bank voles and yellow‐necked mice could thus contribute to the difference in resistance to B. afzelii between the species. This study provides knowledge of gene expression induced by a zoonotic pathogen in its natural host, and possible species‐specific regulation of immune responses associated with resistance.

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Section: Discussionsupporting

confidence: 89%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Comparison of spleen transcriptomes of two wild rodent species reveals differences in the immune response against Borrelia afzelii

Zhong

Lundberg

Råberg

2020

Ecology and Evolution

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“…An enclosure study on bank voles found subtle effects of B. afzelii infection on host reproduction but not on host survival (60). Numerous studies have shown that infection with B. burgdorferi induces pathology (e.g., arthritis and carditis) in laboratory mice (Mus musculus) (61-63) but not in wild rodents (20,35,64,65). Interestingly, young individuals are more likely to develop disease than old individuals (34,35), suggesting that maternally transmitted antibodies increase offspring fitness by delaying pathogen acquisition to an older and more disease-resistant host age class.…”

Section: Discussionmentioning

confidence: 99%

Maternal Antibodies Provide Bank Voles with Strain-Specific Protection against Infection by the Lyme Disease Pathogen

Gomez-Chamorro

Heinrich

Sarr

et al. 2019

Appl Environ Microbiol

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Multistrain microbial pathogens often induce strain-specific antibody responses in their vertebrate hosts. Mothers can transmit antibodies to their offspring, which can provide short-term, strain-specific protection against infection. Few experimental studies have investigated this phenomenon for multiple strains of zoonotic pathogens occurring in wildlife reservoir hosts. The tick-borne bacterium Borrelia afzelii causes Lyme disease in Europe and consists of multiple strains that cycle between the tick vector (Ixodes ricinus) and vertebrate hosts, such as the bank vole (Myodes glareolus). We used a controlled experiment to show that female bank voles infected with B. afzelii via tick bite transmit protective antibodies to their offspring. To test the specificity of protection, the offspring were challenged using a natural tick bite challenge with either the maternal strain to which the mothers had been exposed or a different strain. The maternal antibodies protected the offspring against a homologous infectious challenge but not against a heterologous infectious challenge. The offspring from the uninfected control mothers were equally susceptible to both strains. Borrelia outer surface protein C (OspC) is an antigen that is known to induce strain-specific immunity. Maternal antibodies in the offspring reacted more strongly with homologous than with heterologous recombinant OspC, but other antigens may also mediate strain-specific immunity. Our study shows that maternal antibodies provide strain-specific protection against B. afzelii in an ecologically important rodent reservoir host. The transmission of maternal antibodies may have important consequences for the epidemiology of multistrain pathogens in nature. IMPORTANCE Many microbial pathogen populations consist of multiple strains that induce strain-specific antibody responses in their vertebrate hosts. Females can transmit these antibodies to their offspring, thereby providing them with short-term strain-specific protection against microbial pathogens. We investigated this phenomenon using multiple strains of the tick-borne microbial pathogen Borrelia afzelii and its natural rodent reservoir host, the bank vole, as a model system. We found that female bank voles infected with B. afzelii transmitted to their offspring maternal antibodies that provided highly efficient but strain-specific protection against a natural tick bite challenge. The transgenerational transfer of antibodies could be a mechanism that maintains the high strain diversity of this tick-borne pathogen in nature.

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Getting under the birds’ skin: tissue tropism of Borrelia burgdorferi s.l. in naturally and experimentally infected avian hosts

et al. 2019

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Wild birds are frequently exposed to the zoonotic tick-borne bacteria Borrelia burgdorferi sensu lato (s.l.), and some bird species act as reservoirs for some Borrelia genospecies. Studying the tropism of Borrelia in the host, how it is sequestered in different organs, and whether it is maintained in circulation and/or in the host's skin is important to understand pathogenicity, infectivity to vector ticks and reservoir competency.We evaluated tissue dissemination of Borrelia in blackbirds (Turdus merula) and great tits (Parus major), naturally and experimentally infected with Borrelia genospecies from enzootic foci. We collected both minimally invasive biological samples (feathers, skin biopsies and blood) and skin, joint, brain and visceral tissues from necropsied birds. Infectiousness of the host was evaluated through xenodiagnoses and infection rates in fed and moulted ticks. Skin biopsies were the most reliable method for assessing avian hosts' Borrelia infectiousness, which was supported by the agreement of infection status results obtained from the analysis of chin and lore skin samples from necropsied birds and of their xenodiagnostic ticks, including a significant correlation between the estimated concentration of Borrelia genome copies in the skin and the Borrelia infection rate in the xenodiagnostic ticks. This confirms a dermatropism of Borrelia garinii, B. valaisiana and B. turdi in its avian hosts. However, time elapsed from exposure to Borrelia and interaction between host species and Borrelia genospecies may affect the reliability of skin biopsies. The blood was not useful to assess infectiousness of birds, even during the period of expected maximum spirochetaemia. From the tissues sampled (foot joint, liver, spleen, heart, kidney, gut and brain), Borrelia was detected only in the gut, which could be related with infection mode, genospecies competition, genospecies-specific seasonality and/or excretion processes. Keywords Microorganism tropism . Avian reservoir hosts . Tick-borne pathogens . Lyme borreliosis . Skin biopsies * Ana Cláudia Norte

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Colonization and pathology of Borrelia afzelii in its natural hosts

Cited by 12 publications

References 53 publications

Comparison of spleen transcriptomes of two wild rodent species reveals differences in the immune response against Borrelia afzelii

Comparison of spleen transcriptomes of two wild rodent species reveals differences in the immune response against Borrelia afzelii

Maternal Antibodies Provide Bank Voles with Strain-Specific Protection against Infection by the Lyme Disease Pathogen

Getting under the birds’ skin: tissue tropism of Borrelia burgdorferi s.l. in naturally and experimentally infected avian hosts

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