Abstract
Context
Pathogens can manipulate microbial interactions to ensure survival, potentially altering the functional patterns and microbiome assembly. The present study investigates how Anaplasma phagocytophilum infection affects the functional diversity, composition, and assembly of the Ixodes scapularis microbiome, with a focus on high central pathways—those characterized by elevated values in centrality metrics such as eigenvector, betweenness, and degree measures, in the microbial community.
Methods
Using previously published data from nymphs’ gut V4 region’s amplicons of bacterial 16S rRNA, we predicted the functional diversity and composition in control and A. phagocytophilum-infected ticks and inferred co-occurrence networks of taxa and ubiquitous pathways in each condition to associate the high central pathways to the microbial community assembly.
Results
Although no differences were observed concerning pathways richness and diversity, there was a significant impact on taxa and functional assembly when ubiquitous pathways in each condition were filtered. Moreover, a notable shift was observed in the microbiome’s high central functions. Specifically, pathways related to the degradation of nucleosides and nucleotides emerged as the most central functions in response to A. phagocytophilum infection. This finding suggests a reconfiguration of functional relationships within the microbial community, potentially influenced by the pathogen’s limited metabolic capacity. This limitation implies that the tick microbiome may provide additional metabolic resources to support the pathogen’s functional needs.
Conclusions
Understanding the metabolic interactions within the tick microbiome can enhance our knowledge of pathogen colonization mechanisms and uncover new disease control and prevention strategies. For example, certain pathways that were more abundant or highly central during infection may represent potential targets for microbiota-based vaccines.
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Data availability
The datasets analyzed during the current study were generated by Abraham et al. (2017) and are available in the SRA repository, (https://www.ncbi.nlm.nih.gov/sra/PRJNA353730).
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Funding
This work was supported by the following Brazilian research agencies: FAPERJ (grant E-26/211.312/2021), and CNPq (grant 313753/2021–0). The first author is funded by the National Council for Scientific and Technological Development – CNPq (grant #200528/2022–0). UMR BIPAR is supported by the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence “Integrative Biology of Emerging Infectious Diseases” (grant no. ANR-10-LABX-62-IBEID). Apolline Maitre is supported by the “Collectivité de Corse” grant: “Formations superieures” (SGCE – RAPPORT No 0300).
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ACC and PGP conceptualized and conceived the idea. PGP, LAD, EPS, AM, DO, and ACC analyzed data and/or interpreted the results. PGP and ACC drafted the first version of the manuscript. PGP, LAD, EPS, AM, DO, ACC, and HAS reviewed, edited, and approved the manuscript.
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Paulino, P.G., Abuin-Denis, L., Maitre, A. et al. Dissecting the impact of Anaplasma phagocytophilum infection on functional networks and community stability of the tick microbiome. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00473-8
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DOI: https://doi.org/10.1007/s10123-023-00473-8