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Variation of bacterial community assembly over developmental stages and midgut of Dermanyssus gallinae

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Abstract

Bacterial microbiota play an important role in the fitness of arthropods, but the bacterial microflora in the parasitic mite Dermanyssus gallinae is only partially explored; there are gaps in our understanding of the microbiota localization and in our knowledge of microbial community assembly. In this work, we have visualized, quantified the abundance, and determined the diversity of bacterial occupancy, not only across developmental stages of D. gallinae, but also in the midgut of micro-dissected female D. gallinae mites. We explored community assembly and the presence of keystone taxa, as well as predicted metabolic functions in the microbiome of the mite. The diversity of the microbiota and the complexity of co-occurrence networks decreased with the progression of the life cycle. However, several bacterial taxa were present in all samples examined, indicating a core symbiotic consortium of bacteria. The relatively higher bacterial abundance in adult females, specifically in their midguts, implicates a function linked to the biology of D. gallinae mites. If such an association proves to be important, the bacterial microflora qualifies itself as an acaricidal or vaccine target against this troublesome pest.

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Acknowledgements

We are thankful to the International Poultry Testing Station in Ústrašice (Czech Republic) for providing us with freshly collected mites.

Funding

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). AWC was supported by the Programa Nacional de Becas de Postgrado en el Exterior “Don Carlos Antonio López” (grant no. 205/2018). AM is supported by the “Collectivité de Corse”, grant: “Formations superieures” (SGCE – RAPPORT N° 0300). JP was supported by the Czech Science Foundation grant nos. 22-18424 M and 22-12648 J.

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Author notes

  1. Alejandro Cabezas-Cruz and Jan Perner contributed equally to this work.

Authors and Affiliations

  1. ANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, France

    Alejandra Wu-Chuang, Apolline Maitre, Lourdes Mateos-Hernández & Alejandro Cabezas-Cruz

  2. Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 37005, Ceske Budejovice, Czech Republic

    David Hartmann, Helena Frantová, Veronika Urbanová & Jan Perner

  3. INRAE, UR 0045 Laboratoire de Recherches Sur Le Développement de L’Elevage (SELMET-LRDE), 20250, Corte, France

    Apolline Maitre

  4. EA 7310, Laboratoire de Virologie, Université de Corse, Corte, France

    Apolline Maitre

  5. School of Environmental Sciences, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Dasiel Obregon

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  1. Alejandra Wu-Chuang
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Contributions

A.W.C.: microbiome data analysis and drafting of the manuscript; D.H.: data acquisition (sorting of mites and DNA extraction); A.M.: drafting of the manuscript; L.M.H.: microbiome data processing; H.F.: data acquisition (PCR); V.U.: data acquisition (fluorescence in situ hybridisation); D.O.: software; A.C.C. and J.P. conceived the research, designed the experiments and wrote the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Alejandro Cabezas-Cruz or Jan Perner.

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Supplementary Information

Supplementary Fig. S1

Microscope image of dissection of D. gallinae midgut. Sequential images of the micro-dissection of midguts from adult D. gallinae females. (PNG 2607 kb)

High resolution image (TIF 25238 kb)

Supplementary Fig. S2

Keystone taxa of D. gallinae across life stages. Scatter plot showing the mean relative abundance (expressed as clr) and the eigenvector centrality of each bacterial taxon (dots or diamonds) of the microbial community of red mites at the stages of (A) eggs, larvae and protonymphs, (B) nymphs, (C) adult males and (D) adult females. Green dots or diamonds represent ubiquitous bacteria (i.e., taxa that were found across all the samples). A cutoff value of 5 was set for the mean relative abundance and 0.75 for the eigenvector centrality. Ubiquitous bacterial taxa with mean relative abundanceand eigenvector centrality equal to or higher than the cutoff values were considered as keystone taxa (Green diamonds). List of keystone taxa is displayed next to the scatterplot (PNG 165 kb)

High resolution image (TIF 10434 kb)

Supplementary Fig. S3

Uniqueor shared pathways with differential abundance in red mites at different life stages. Venn diagram showing the number of common and unique pathways whose abundance changed significantly between comparisons of eggs, larvae and protonymphs vs. nymphs, adult male vs. nymphs and adult femalevs. nymphs. (PNG 51 kb)

High resolution image (TIF 2817 kb)

Supplementary Table S1

Relative quantification of 16S rDNA of different life stages of D. gallinae. (DOCX 15 kb)

Supplementary Table S2

Bacterial taxa found as contaminants in the 16S rDNA gene sequencing datasets from red mites at different life stages. Contaminants were statistically identified (TRUE) and removed from the 16S rDNA gene sequencing datasets using the decontam R package. (XLS 1244 kb)

Supplementary Table S3

Unique or shared bacterial taxa among the life stages and in adult female gut of red mites. (XLSX 31 kb)

Supplementary Table S4

Unique or shared nodes in microbial co-occurrence networks among the life stages of red mites. (XLSX 21 kb)

Supplementary Table S5

Jaccard indexes of local centrality measures. Jaccard’s indexes for each of local centrality measures (i.e., degree, betweenness centrality, closeness centrality, eigenvector centrality and hub taxa) of the sets of most central nodes for pairwise network comparisons. The two p-values, P(J ≤ j) and P(J ≥ j), for each Jaccard’s index were added. (XLSX 17 kb)

Supplementary Table S6

List of bacterial taxa from the total diversity that can be found as a node in the microbial co-occurrence networks at different life stages of red mites. (XLSX 45 kb)

Supplementary Table S7

Predicted pathways shared between the different life stages of red mites. (XLSX 28 kb)

Supplementary Table S8

Pathways with differential abundance in red mites at different life stages. (XLSX 49 kb)

Supplementary Table S9

Unique or shared pathways with differential abundance in red mites at different life stages. (XLSX 16 kb)

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Wu-Chuang, A., Hartmann, D., Maitre, A. et al. Variation of bacterial community assembly over developmental stages and midgut of Dermanyssus gallinae. Microb Ecol 86, 2400–2413 (2023). https://doi.org/10.1007/s00248-023-02244-4

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