Rickettsia helvetica infection is associated with microbiome modulation in Ixodes ricinus collected from humans in Serbia

• Published in: Scientific reports Vol. 12; no. 1; p. 11464
• Main Authors: Maitre, Apolline, Wu-Chuang, Alejandra, Mateos-Hernández, Lourdes, Foucault-Simonin, Angélique, Moutailler, Sara, Paoli, Jean-Christophe, Falchi, Alessandra, Díaz-Sánchez, Adrian A., Banović, Pavle, Obregón, Dasiel, Cabezas-Cruz, Alejandro
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 06-07-2022; Nature Publishing Group; Nature Portfolio
• Subjects: 631/326/2565; 631/326/41; 631/326/421; Arachnids; Disease control; Fever; Humanities and Social Sciences; Infections; Ixodes ricinus; Life Sciences; Metabolic pathways; Metabolism; Microbial activity; Microbiomes; Microbiota; Midgut; multidisciplinary; Pathogens; Rickettsia; Rickettsia helvetica; Salivary gland; Science; Science (multidisciplinary); Serbia
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-022-15681-x

Rickettsia helvetica
is an emerging pathogen of the Spotted Fever Group Rickettsia (SFGR) causing spotted fever diseases in various European countries. This tick-borne pathogen replicates in tick tissues such as the midgut and salivary gland, but its potential interactions with the vector microbiota is poorly characterized. The vector microbiome plays a pivotal role in tick-pathogen interactions, and some microbiota members facilitate or impede tick-borne pathogen infection. Manipulations of the tick microbiome have led to reduction in pathogen colonization in the tick vector. However, translating these findings into disease control applications requires a thorough characterization of vector microbiota response to different pathogens. In this study, we analyzed and compared the microbiota of
Ixodes ricinus
ticks attached on humans and collected in Serbia. Ticks were either infected with
R. helvetica
, or uninfected with major tick-borne pathogens (referred hereafter as ‘pathogen-free’). We used microbial co-occurrence network analysis to determine keystone taxa of each set of samples, and to study the interaction patterns of the microbial communities in response to pathogen infection. The inferred functional profiles of the tick microbiome in
R. helvetica
-positive and pathogen-free samples were also compared. Our results show that
R. helvetica
infection reduces significantly the diversity of the microbiota and the connectivity of the co-occurrence network. In addition, using co-occurrence network we identified bacterial taxa (i.e., Enterobacteriaceae, Comamonadaceae, and
Bacillus
) that were negatively associated with ‘
Rickettsia
’ in
R. helvetica
-infected ticks, suggesting competition between
R. helvetica
and some members of the tick microbiota. The reconstruction of microbial metabolic pathways shows that the presence of
R. helvetica
might have a major impact on the metabolic functions of the tick microbiome. These results can inform novel interventions for the prevention of
R. helvetica
, or other SFGR infections in humans.