Ticks are obligate, bloodsucking, nonpermanent ectoparasitic arthropods. Among them, Ixodes ricinus is a classic example of an extreme generalist tick, presenting a highly permissive feeding behavior using different groups of vertebrates as hosts, such as mammalian (including humans), avian and reptilian species (Hoogstraal & Aeschlimann, 1982; Dantas-Torresa & Otranto, 2013). This ecological adaptation can account for the broad geographical distribution of I. ricinus populations, which extends from the western end of the European continent to the Ural Mountains in Russia, and from northern Norway to the Mediterranean basin, including the North African countries - Morocco, Algeria and Tunisia (https://ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/tick-maps). The contact with different hosts also promotes the exposure/acquisition and transmission of various pathogenic agents (viruses, bacteriae, protists and nematodes) of veterinary and medical relevance (Aeschlimann et al., 1979). As one of the prime ticks found on humans, this species is implicated in diseases such as Lyme borreliosis, Spotted Fever Group rickettsiosis, Human Anaplasmosis, Human Babesiosis and Tick-borne Encephalitis (Velez et al., 2023). 

The climate change projections drawn for I. ricinus, in the scenario of global warming, point for the expansion/increase activity in both latitude and altitude (Medlock et al., 2013). The adequacy of vector modeling is relaying in the proper characterization of complex biological systems. Thus, it is essential to increase knowledge on I. ricinus, focusing on aspects such as genetic background, ecology and eco-epidemiology on a microscale but also at a country and region level, due to possible local adaptations of tick populations and genetic drift. 

In the present systematic revision, Perez et al. (2023) combine old and recently published data (mostly up to 2020) regarding I. ricinus distribution, phenology, host range and pathogen association in continental France and Corsica Island. Based on a keyword search of peer-reviewed papers on seven databases, as well as other sources of grey literature (mostly, thesis), the authors have synthesized information on: 1) Host parasitism to detect potential differences in host use comparing to other areas in Europe; 2) The spatiotemporal distribution of I. ricinus, to identify possible geographic trends in tick density, variation in activity patterns and the influence of environmental factors; 3) Tick-borne pathogens detected in this species, to better assess their spatial distribution and variation in exposure risk. 

As pointed out by both reviewers, this work clearly summarizes the information regarding I. ricinus and associated microorganisms from European France. This review also identifies remaining knowledge gaps, providing a comparable basis to orient future research. This is why I chose to recommend Perez et al (2023)'s preprint for Peer Community Infections. 

REFERENCES

Aeschlimann, A., Burgdorfer, W., Matile, H., Peter, O., Wyler, R. (1979) Aspects nouveaux du rôle de vecteur joué par Ixodes ricinus L. en Suisse. Acta Tropica, 36, 181-191.

Dantas-Torresa, F., Otranto, D. (2013) Seasonal dynamics of Ixodes ricinus on ground level and higher vegetation in a preserved wooded area in southern Europe. Veterinary Parasitology, 192, 253- 258.
https://doi.org/10.1016/j.vetpar.2012.09.034

Hoogstraal, H., Aeschlimann, A. (1982) Tick-host specificity. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 55, 5-32.

Medlock, J.M., Hansford, K.M., Bormane, A., Derdakova, M., Estrada-Peña, A., George, J.C., Golovljova, I., Jaenson, T.G.T., Jensen, J.K., Jensen, P.M., Kazimirova, M., Oteo, J.A., Papa, A., Pfister, K., Plantard, O., Randolph, S.E., Rizzoli, A., Santos-Silva, M.M., Sprong, H., Vial, L., Hendrickx, G., Zeller, H., Van Bortel, W. (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites and Vectors, 6. https://doi.org/10.1186/1756-3305-6-1

Perez, G., Bournez, L., Boulanger, N., Fite, J., Livoreil, B., McCoy, K., Quillery, E., René-Martellet, M., Bonnet, S. (2023) The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review. bioRxiv, ver. 1 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.04.18.537315

Velez, R., De Meeûs, T., Beati, L., Younsi, H., Zhioua, E., Antunes, S., Domingos, A., Ataíde Sampaio, D., Carpinteiro, D., Moerbeck, L., Estrada-Peña, A., Santos-Silva, M.M., Santos, A.S. (2023) Development and testing of microsatellite loci for the study of population genetics of Ixodes ricinus Linnaeus, 1758 and Ixodes inopinatus Estrada-Peña, Nava & Petney, 2014 (Acari: Ixodidae) in the western Mediterranean region. Acarologia, 63, 356-372. https://doi.org/10.24349/bvem-4h49

Most plant-infecting viruses rely on an animal vector to be transmitted from one sessile host plant to another. A fascinating aspect of virus-vector interactions is the fact that viruses from different clades produce different proteins to bind vector receptors (1). Two major processes are described. In the “capsid strategy”, a motif of the capsid protein is directly binding to the vector receptor. In the “helper strategy”, a non-structural component, the helper component (HC), establishes a bridge between the virus particle and the vector’s receptor.   

In this exhaustive review focusing on hemipteran insect vectors, Di Mattia et al. (2) are revisiting the helper strategy in light of recent results. The authors first place the discoveries of the HC strategy in a historical context, suggesting that HC are exclusively found in non-circulative viruses (viruses that only attach to the vector). They present an overview of the nature and modes of action of helper components in the major virus clades of non-circulative viruses (Potyviruses and Caulimoviruses). Authors then detail recent advances, to which they have significantly contributed, showing that the helper strategy also appears widespread in circulative transmission categories (Tenuiviruses, Nanoviruses). 

In an extensive perspective section, they raise the question of the evolutionary significance of the existence of HC in numerous unrelated viruses, transmitted by unrelated vectors through different mechanisms. They explore the hypothesis that the helper strategy evolved several times independently in distinct viral clades and for different reasons. In particular, they present several potential benefits of plant virus HC related to virus cooperation, collective transmission and effector-driven infectivity.

As pointed out by both reviewers, this is a very clear and synthetic review. Di Mattia et al. present an exhaustive overview of virus HC-vector molecular interactions and address functionally and evolutionarily important questions. This review should benefit a large audience interested in host-virus interactions and transmission processes.

REFERENCES

(1) Ng JCK, Falk BW (2006) Virus-Vector Interactions Mediating Nonpersistent and Semipersistent Transmission of Plant Viruses. Annual Review of Phytopathology, 44, 183–212. https://doi.org/10.1146/annurev.phyto.44.070505.143325

(2) Di Mattia J, Zeddam J-L, Uzest M, Blanc S (2023) The helper strategy in vector-transmission of plant viruses. Zenodo, ver. 2 peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.5281/zenodo.7709290

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

The impact of virus infection of a plant on an aphid’s behaviour has been observed in many studies [1]. Indeed, virus infection can alter plant biochemistry through the emission of volatile organic compounds and plant tissue content modification. These alterations can further impact the interactions between plants and aphids. However, although it is a well-known phenomenon, very few studies have explored the consequences of plant virus infection on the gene expression of aphids to understand better the aphid’s manipulation by the plant virus. In this context, the recommended study [2] reports a comprehensive transcriptomic analysis of the genes expressed by one aphid species, Myzus persicae, a vector of several plant viruses, when feeding on plants. Michelle Heck underlined how significant this study is for comprehending the molecular bases of aphid-vector manipulation by plant viruses (see below).

Interestingly, the study design has integrated several factors that might influence the gene expression of M. persicae when feeding on the plant. Indeed, the authors investigated the effect of two plant species (Arabidopsis thaliana and Camelia sativa) and two virus species [turnip yellows virus (TuYV) and cauliflower mosaic virus (CaMV)]. Noteworthy, the transmission mode of TuYV is circulative and persistent, while CaMV is transmitted by a semi-persistent non-circulative mode. As Juan José Lopez Moya mentioned, multiple comparisons allowed the identification of the different responses of aphids in front of different host plants infected or not by different viruses (see below). This publication is complementary to a previous publication from the same team focusing on plant transcriptome analysis [3].

Thanks to their experimental design, the authors identified genes commonly deregulated by both viruses and/or both plant species and deregulated genes by a single virus or a single plant. Figure 4 nicely summarizes the number of deregulated genes. A thorough discussion on the putative role of deregulated genes in different conditions gave a comprehensive follow-up of the results and their impact on the current knowledge of plant-virus-vector interactions.

This study has now opened the gate to promising research focusing on the functional validation of the identified genes while also narrowing the study from the body to the tissue level.

References:

1. Carr JP, Tungadi T, Donnelly R, Bravo-Cazar A, Rhee S-J, Watt LG, Mutuku JM, Wamonje FO, Murphy AM, Arinaitwe W, Pate AE, Cunniffe NJ, Gilligan CA (2020) Modelling and manipulation of aphid-mediated spread of non-persistently transmitted viruses. Virus Research, 277, 197845. https://doi.org/10.1016/j.virusres.2019.197845

2. Chesnais Q, Golyaev V, Velt A, Rustenholz C, Verdier M, Brault V, Pooggin MM, Drucker M (2022) Transcriptome responses of the aphid vector Myzus persicae are shaped by identities of the host plant and the virus. bioRxiv , 2022.07.18.500449, ver. 5 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.07.18.500449

3. Chesnais Q, Golyaev V, Velt A, Rustenholz C, Brault V, Pooggin MM, Drucker M (2022) Comparative Plant Transcriptome Profiling of Arabidopsis thaliana Col-0 and Camelina sativa var. Celine Infested with Myzus persicae Aphids Acquiring Circulative and Noncirculative Viruses Reveals Virus- and Plant-Specific Alterations Relevant to Aphid Feeding Behavior and Transmission. Microbiology Spectrum, 10, e00136-22. https://doi.org/10.1128/spectrum.00136-22

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