Worldwide, ticks and tick-borne diseases are a persistent example of problems at the One Health interface between humans, wildlife, and environment (1, 2). The management and prevention of ticks and tick-borne diseases require a better understanding of host, tick and pathogen interactions and thus get a better view of the tick-borne pathosystems.

In this study (3), the tick-borne pathosystem included three component species: first a seabird host, the Yellow-legged gull (YLG - Larus michahellis, Laridae), second a soft nidicolous tick (Ornithodoros maritimus, Argasidae, syn. Alectorobius maritimus) known to infest this host and third a blood parasite (Babesia sp. YLG, Piroplasmidae). In this pathosystem, authors investigated the role of the soft tick, Ornithodoros maritimus, as a potential vector of Babesia sp. YLG. They analyzed the transmission of Babesia sp. YLG by collecting different tick life stages from YLG nests during 4 consecutive years on the islet of Carteau (Gulf of Fos, Camargue, France). Ticks were dissected and organs were analyzed separately to detect the presence of Babesia sp DNA and to evaluate different transmission pathways.

While the authors detected Babesia sp. YLG DNA in the salivary glands of nymphs, females and males, this result reveals a strong suspicion of transmission of the parasite by the soft tick. Babesia sp. YLG DNA was also found in tick ovaries, which could indicate possible transovarial transmission. Finally, the authors detected Babesia sp. YLG DNA in several male testes and in endospermatophores, and notably in a parasite-free female (uninfected ovaries and salivary glands). These last results raise the interesting possibility of sexual transmission from infected males to uninfected females.

As pointed out by both reviewers, this is a nice study, well written and easy to read. All the results are new and allow to better understand the role of the soft tick, Ornithodoros maritimus, as a potential vector of Babesia sp. YLG. They finally question about the degree to which the parasite can be maintained locally by ticks and the epidemiological consequences of infection for both O. maritimus and its avian host. For all these reasons, I chose to recommend this article for Peer Community In Infections.

References

1. Dantas-Torres et al (2012). Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol. 28:437. https://doi.org/10.1016/j.pt.2012.07.003 
2. Johnson N et al (2022). One Health Approach to Tick and Tick-Borne Disease Surveillance in the United Kingdom. Int J Environ Res Public Health. 19:5833. https://doi.org/10.3390/ijerph19105833
3. Bonsergent C, Vittecoq M, Leray C, Jouglin M, Buysse M, McCoy KD, Malandrin L. A soft tick vector of Babesia sp. YLG in Yellow-legged gull (Larus michahellis) nests. bioRxiv, 2023.03.24.534071, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.03.24.534071

The gut of vertebrates is a host for hundreds or thousands of different species of microorganisms named the gut microbiome. This latter may differ greatly in natural environments between individuals, populations and species (1). The vertebrate gut microbiome plays key roles in host fitness through functions including nutrient acquisition, immunity and defense against infectious agents. While bank voles are small mammals potentially reservoirs of a large number of infectious agents, questions about the links between their gut microbiome and the presence of pathogens are scarcely addressed. 

In this study, Bouilloud et al. (2) used complementary analyses of community and microbial ecology to (i) assess the variability of gut bacteriome diversity and composition in wild populations of the bank vole Myodes glareolus collected in four different sites in Eastern France and (ii) evaluate the three-way interactions between the gut bacteriota, the gastro-intestinal helminths and pathogenic bacteria detected in the spleen. Authors identified important variations of the gut bacteriota composition and diversity among bank voles mainly explained by sampling localities. They found positive correlations between the specific richness of both the gut bacteria and the helminth community, as well as between the composition of these two communities, even when accounting for the influence of geographical distance. The helminths Aonchotheca murissylvatici, Heligmosomum mixtum and the bacteria Bartonella sp were the main taxa associated with the whole gut bacteria composition. Besides, changes in relative abundance of particular gut bacterial taxa were specifically associated with other helminths (Mastophorus muris, Catenotaenia henttoneni, Paranoplocephala omphalodes and Trichuris arvicolae) or pathogenic bacteria. Infections with Neoehrlichia mikurensis, Orientia sp, Rickettsia sp and P. omphalodes were especially associated with lower relative abundance of members of the family Erysipelotrichaceae (Firmicutes), while coinfections with higher number of bacterial infections were associated with lower relative abundance of members of the Bacteroidales family (Bacteroidetes). 

As pointed out by both reviewers, this study represents a significant advance in the field. I would like to commend the authors for this enormous work. The amount of data, analyses and results is considerable which has sometimes complicated the understanding of the story at the beginning of the evaluation process. Thanks to constructive scientific interactions with both reviewers through the two rounds of evaluation, the authors have efficiently addressed the reviewer's concerns and improved the manuscript, making this great story easier to read. The innovative results of this study emphasize the complex interlinkages between gut bacteriome and infections in wild animal populations and I strongly recommend this article for publication In Peer Community Infections. 

References

(1) Vujkovic-Cvijin I, Sklar J, Jiang L, Natarajan L, Knight R, Belkaid Y (2020) Host variables confound gut microbiota studies of human disease. Nature, 587, 448–454. https://doi.org/10.1038/s41586-020-2881-9

(2) Bouilloud M, Galan M, Dubois A, Diagne C, Marianneau P, Roche B, Charbonnel N (2023) Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populations. biorxiv, 2022.05.23.493084, ver. 2 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.05.23.493084

As recently reported by the world organisation for animal health, 60% of infectious diseases are zoonotic with a significant part associated to ticks. Ticks can transmit various pathogens such as bacteria, viruses and parasites. Among pathogens known to be transmitted by ticks, Ehrlichia ruminantium is an obligate intracellular Gram-negative bacterium responsible for the fatal heartwater disease of domestic and wild ruminants (Allsopp, 2010). E. ruminantium is transmitted by ticks of the genus Amblyomma in the tropical and sub-Saharan areas, as well as in the Caribbean islands. It constitutes a major threat for the American livestock industries since a suitable tick vector is already present in the American mainland and potential introduction of infected A. variegatum through migratory birds or uncontrolled movement of animals from Caribbean could occur (i.e. Deem, 1998 ; Kasari et al 2010). The disease is also a major obstacle to the introduction of animals from heartwater-free to heartwater-infected areas into sub-Saharan Africa and thus restrains breeding programs aiming at upgrading local stocks (Allsopp, 2010).

In this context, it is essential to develop control strategies against heartwater, as developing effective vaccines, for instance. Such an objective requires a better understanding of the early interaction of E. ruminantium and its host cells and of the mechanisms associated with bacterial adhesion to the host-cell. In this study, the authors. studied the role of E. ruminantium membrane protein ERGA_CDS_01230 in the adhesion process to host bovine aortic endothelial cells (BAEC).

After successfully producing the recombinant version of the protein, Pinarello et al (2022) followed the in vitro culture of E. ruminantium in BAEC and observed that the expression of the protein peaked at the extracellular infectious elementary body stages. This result would suggest the likely involvement of the protein in the early interaction of E. ruminantium with its host cells. The authors then showed using flow cytometry, and scanning electron microscopy, that beads coated with the recombinant protein adhered to BAEC. In addition, they also observed that the adhesion protein of E. ruminantium interacted with proteins of the cell's lysate, membrane and organelle fractions. Additionally, enzymatic treatment, degrading dermatan and chondroitin sulfates on the surface of BAEC, was associated with a 50% reduction in the number of bacteria in the host cell after a development cycle, indicating that glycosaminoglycans might play a role in the adhesion of E. ruminantium to the host-cell. Finally, the authors observed that the adhesion protein of E. ruminantium induced a humoral response in vaccinated animals, making this protein a possible vaccine candidate.

As rightly pointed out by both reviewers, the results of this study represent a significant advance (i) in the understanding of the role of the E. ruminantium membrane protein ERGA_CDS_01230 in the adhesion process to the host-cell and (ii) in the development of new control strategies against heartwater as this protein might potentially be used as an immunogen for the development of future vaccines.

References

Allsopp, B.A. (2010). Natural history of Ehrlichia ruminantium. Vet Parasitol 167, 123-135. https://doi.org/10.1016/j.vetpar.2009.09.014

Deem, S.L. (1998). A review of heartwater and the threat of introduction of Cowdria ruminantium and Amblyomma spp. ticks to the American mainland. J Zoo Wildl Med 29, 109-113.

Kasari, T.R. et al (2010). Recognition of the threat of Ehrlichia ruminantium infection in domestic and wild ruminants in the continental United States. J Am Vet Med Assoc. 237:520-30. https://doi.org/10.2460/javma.237.5.520

Pinarello V, Bencurova E, Marcelino I, Gros O, Puech C, Bhide M, Vachiery N, Meyer DF (2022) Ehrlichia ruminantium uses its transmembrane protein Ape to adhere to host bovine aortic endothelial cells. bioRxiv, 2021.06.15.447525, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2021.06.15.447525