Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

Narasimhan, Sukanya; Schuijt, Tim J.; Abraham, Nabil M.; Rajeevan, Nallakkandi; Coumou, Jeroen; Graham, Morven; Robson, Andrew; Wu, Ming-Jie; Daffre, Sirlei; Hovius, Joppe W.; Fikrig, Erol

doi:10.1038/s41467-017-00208-0

Cited by 91 publications

(147 citation statements)

References 73 publications

(107 reference statements)

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“…Ixodes scapularis harbors a diverse group of native microbes, ranging from viruses to bacteria [2]. These microbial communities influence the ability of B. burgdorferi and A. phagocytophilum to colonize and persist within the vector [3][4][5]. Microbial biofilms [6], generated by symbiotic relationships in arthropod hosts [7,8].…”

Section: Introductionmentioning

confidence: 99%

“…Microbial biofilms [6], generated by symbiotic relationships in arthropod hosts [7,8]. Borrelia burgdorferi and A. phagocytophilum colonization in I. scapularis is associated with changes in the taxonomic composition of the microbiota resulting in diffuse biofilms [3,4]. Tick gene expression is affected by B. burgdorferi and A. phagocytophilum infection in I. scapularis gut.…”

Section: Introductionmentioning

confidence: 99%

“…Tick gene expression is affected by B. burgdorferi and A. phagocytophilum infection in I. scapularis gut. A secreted protein with a Reeler domain (PIXR) and an antifreeze glycoprotein (IAFGP) with antimicrobial properties are upregulated by B. burgdorferi and A. phagocytophilum, respectively [3,4,9]. The IAFGP and the anti-PIXR immunity also alter the tick microbiota and result in diffuse and dense biofilms, respectively [3,4].…”

Section: Introductionmentioning

confidence: 99%

“…We hypothesized that these disturbing factors induce taxonomic and functional changes that impact the resistance of tick microbiota, and may explain the properties of two set of biofilms that we named α and β ( Figure 1). Anti-tick immunity results in a microbial community that increases biofilms in the tick gut [4], referred hereafter as biofilm α, b) disturbance of tick gut microbial communities by A. phagocytophilum infection [3], and c) antimicrobial peptide treatment [3,9], produces scattered and fragmented bacterial biofilms, refereed hereafter as biofilms β1 and β1, respectively.…”

Section: Introductionmentioning

confidence: 99%

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Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides

2020

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Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins, which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis antifreeze glycoprotein (IAFGP), a protein with antimicrobial activity, while Borrelia burgdorferi induces the expression of PIXR. Here, we tested the resistance of I. scapularis microbiome to A. phagocytophilum infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. We demonstrate that A. phagocytophilum infection and IAFGP affect the taxonomic composition and taxa co-occurrence networks, but had limited impact on the functional traits of tick microbiome. In contrast, anti-tick immunity disturbed the taxonomic composition and the functional profile of tick microbiome, by increasing both the taxonomic and pathways diversity. Mechanistically, we show that anti-tick immunity increases the representation and importance of the polysaccharide biosynthesis pathways involved in biofilm formation, while these pathways are under-represented in the microbiome of ticks infected by A. phagocytophilum or exposed to IAFGP. These analyses revealed that tick microbiota is highly sensitive to anti-tick immunity, while it is less sensitive to pathogen infection and antimicrobial peptides. Results suggest that biofilm formation may be a defensive response of tick microbiome to anti-tick immunity.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides

2020

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“…Previous studies have shown that spermidine is more abundant in human blood (9 lM) than putrescine (0.13 lM) (Wishart et al, 2007(Wishart et al, , 2009(Wishart et al, , 2013 and is the only polyamine available in the midgut of nymphal ticks. The availability of spermidine in the various hosts and vectors harboring B. burgdorferi and its selective transport strongly suggests that spermidine is the essential polyamine required by B. burgdorferi for survival (Narasimhan et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Borrelia burgdorferi genes, bb0639‐0642, encode a putative putrescine/spermidine transport system, PotABCD, that is spermidine specific and essential for cell survival

Bontemps-Gallo

Lawrence

Richards

et al. 2018

Molecular Microbiology

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Polyamines are an essential class of metabolites found throughout all kingdoms in life. Borrelia burgdorferi harbors no enzymes to synthesize or degrade polyamines yet does contain a polyamine uptake system, potABCD. In this report, we describe the initial characterization of this putative transport system. After several unsuccessful attempts to inactivate potABCD, we placed the operon under the control of an inducible LacI promoter expression system. Analyses of this construct confirmed that potABCD was required for in vitro survival. Additionally, we demonstrated that the potABCD operon were upregulated in vitro by low osmolarity. Previously, we had shown that low osmolarity triggers the activation of the Rrp2/RpoN/RpoS regulatory cascade, which regulates genes essential for the transmission of spirochetes from ticks to mammalian hosts. Interestingly, induction of the pot operon was only affected in an rpoS mutant but not in a rpoN mutant, suggesting that the genes were RpoS dependent and RpoN independent. Furthermore, potABCD was upregulated during tick feeding concomitant with the initiation of spirochete replication. Finally, uptake experiments determined the specificity of B. burgdorferi's PotABCD for spermidine.

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Dynamic nesting of Anaplasma marginale in the microbial communities of Rhipicephalus microplus

Piloto‐Sardiñas,

Abuin‐Denis,

Maitre

et al. 2024

Ecology and Evolution

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Interactions within the tick microbiome involving symbionts, commensals, and tick‐borne pathogens (TBPs) play a pivotal role in disease ecology. This study explored temporal changes in the microbiome of Rhipicephalus microplus, an important cattle tick vector, focusing on its interaction with Anaplasma marginale. To overcome limitations inherent in sampling methods relying on questing ticks, which may not consistently reflect pathogen presence due to variations in exposure to infected hosts in nature, our study focused on ticks fed on chronically infected cattle. This approach ensures continuous pathogen exposure, providing a more comprehensive understanding of the nesting patterns of A. marginale in the R. microplus microbiome. Using next‐generation sequencing, microbiome dynamics were characterized over 2 years, revealing significant shifts in diversity, composition, and abundance. Anaplasma marginale exhibited varying associations, with its increased abundance correlating with reduced microbial diversity. Co‐occurrence networks demonstrated Anaplasma's evolving role, transitioning from diverse connections to keystone taxa status. An integrative approach involving in silico node removal unveils the impact of Anaplasma on network stability, highlighting its role in conferring robustness to the microbial community. This study provides insights into the intricate interplay between the tick microbiome and A. marginale, shedding light on potential avenues for controlling bovine anaplasmosis through microbiome manipulation.

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Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

Cited by 91 publications

References 73 publications

Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides

Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides

Borrelia burgdorferi genes, bb0639‐0642, encode a putative putrescine/spermidine transport system, PotABCD, that is spermidine specific and essential for cell survival

Dynamic nesting of Anaplasma marginale in the microbial communities of Rhipicephalus microplus

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