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21 Sep 2023
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Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potential

Fill in one gap in our understanding of CHIKV intra-vector dynamics

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Mosquitoes are first vector of pathogen worldwide and transmit several arbovirus, most of them leading to major outbreaks (1). Chikungunya virus (CHIKV) is a perfect example of the “explosive type” of arbovirus, as observed in La Réunion Island in 2005-2006 (2-6) and also in the outbreak of 2007 in Italy (7), both vectorized by Ae. albopictus. Being able to better understand CHIKV intra-vector dynamics is still of major interest since not all chikungunya strain are explosive ones (8). 

In this study (9), the authors have evaluated the vector competence of a local strain of Aedes albopictus (collected in Lyon, France) for CHIKV. They evaluated infection, dissemination and transmission dynamics of CHIKV using different dose of virus in individual mosquitoes from day 2 to day 20 post exposure, by titration and quantification of CHIKV RNA load in the saliva. As highlighted by both reviewers, the most innovative idea in this study was the use of three different oral doses trying to span human viraemia detected in two published studies (10-11), doses that were estimated through their model of human CHIKV viremia in the blood.  They have found that CHIKV dissemination from the Ae. albopictus midgut depends on the interaction between time post-exposure and virus dose (already highlighted by other international publications).  Then their results were implemented in the agent-based model nosoi to estimate the epidemic potential of CHIKV in a French population of Ae. albopictus, using realistic vectorial capacity parameters.

To conclude, the authors have discussed the importance of other parameters that could influence vector competence as mosquito microbiota and temperature, parameters that need also to be estimated in local mosquito population to improve the risk assessment through modelling.  

As pointed out by both reviewers, this is a nice study, well written and easy to read. These results allow filling in another gap of our understanding of CHIKV intra-vector dynamics and highlight the epidemic potential of CHIKV upon transmission by Aedes albopictus in mainland France. For all these reasons, I chose to recommend this article for Peer Community In Infections.

References

1.       Marine Viglietta, Rachel Bellone, Adrien Albert Blisnick, Anna-Bella Failloux. (2021). Vector Specificity of Arbovirus Transmission. Front Microbiol Dec 9;12:773211. https://doi.org/10.3389/fmicb.2021.773211

2.       Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney M-C, Lavenir R, Pardigon N, Reynes J-M, Pettinelli F, Biscornet L, Diancourt L, Michel S, Duquerroy S, Guigon G, Frenkiel M-P, Bréhin A-C, Cubito N, Desprès P, Kunst F, Rey FA, Zeller H, Brisse S. (2006). Genome Microevolution of Chikungunya viruses Causing the Indian Ocean Outbreak. 2006. PLoS Medicine, 3, e263. https://doi.org/10.1371/journal.pmed.0030263

3.       Bonilauri P, Bellini R, Calzolari M, Angelini R, Venturi L, Fallacara F, Cordioli P, 687 Angelini P, Venturelli C, Merialdi G, Dottori M. (2008). Chikungunya Virus in Aedes albopictus, Italy. Emerging Infectious 689 Diseases, 14, 852–854. https://doi.org/10.3201/eid1405.071144

4.       Pagès F, Peyrefitte CN, Mve MT, Jarjaval F, Brisse S, Iteman I, Gravier P, Tolou H, Nkoghe D, Grandadam M. (2009). Aedes albopictus Mosquito: The Main Vector of the 2007 Chikungunya Outbreak in Gabon. PLoS ONE, 4, e4691. https://doi.org/10.1371/journal.pone.0004691

5.       Paupy C, Kassa FK, Caron M, Nkoghé D, Leroy EM (2012) A Chikungunya Outbreak Associated with the Vector Aedes albopictus in Remote Villages of Gabon. Vector-Borne and Zoonotic Diseases, 12, 167–169. https://doi.org/10.1089/vbz.2011.0736

6.       Mombouli J-V, Bitsindou P, Elion DOA, Grolla A, Feldmann H, Niama FR, Parra H-J, Munster VJ. (2013). Chikungunya Virus Infection, Brazzaville, Republic of Congo, 2011. Emerging Infectious Diseases, 19, 1542–1543. https://doi.org/10.3201/eid1909.130451

7.       Venturi G, Luca MD, Fortuna C, Remoli ME, Riccardo F, Severini F, Toma L, Manso MD, Benedetti E, Caporali MG, Amendola A, Fiorentini C, Liberato CD, Giammattei R, Romi R, Pezzotti P, Rezza G, Rizzo C. (2017). Detection of a chikungunya outbreak in Central Italy, August to September 2017. Eurosurveillance, 22, 17–00646. https://doi.org/10.2807/1560-7917.es.2017.22.39.17-00646

8.       de Lima Cavalcanti, T.Y.V.; Pereira, M.R.; de Paula, S.O.; Franca, R.F.d.O. (2022). A Review on Chikungunya Virus Epidemiology, Pathogenesis and Current Vaccine Development. Viruses 2022, 14, 969. https://doi.org/10.3390/v14050969

9.       Barbara Viginier, Lucie Cappuccio, Celine Garnier, Edwige Martin, Carine Maisse, Claire Valiente Moro, Guillaume Minard, Albin Fontaine, Sebastian Lequime, Maxime Ratinier, Frederick Arnaud, Vincent Raquin. (2023). Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potential. medRxiv, ver.3, peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2022.11.06.22281997

10.     Appassakij H, Khuntikij P, Kemapunmanus M, Wutthanarungsan R, Silpapojakul K (2013) Viremic profiles in CHIKV-infected cases. Transfusion, 53, 2567–2574. https://doi.org/10.1111/j.1537-2995.2012.03960.x

11.     Riswari SF, Ma’roef CN, Djauhari H, Kosasih H, Perkasa A, Yudhaputri FA, Artika IM, Williams M, Ven A van der, Myint KS, Alisjahbana B, Ledermann JP, Powers AM, Jaya UA (2015) Study of viremic profile in febrile specimens of chikungunya in Bandung, Indonesia. Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology, 74, 61–5. https://doi.org/10.1016/j.jcv.2015.11.017

Chikungunya intra-vector dynamics in *Aedes albopictus* from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potentialBarbara Viginier, Lucie Cappuccio, Celine Garnier, Edwige Martin, Carine Maisse, Claire Valiente Moro, Guillaume Minard, Albin Fontaine, Sebastian Lequime, Maxime Ratinier, Frederick Arnaud, Vincent Raquin<p>Arbovirus emergence and epidemic potential, as approximated by the vectorial capacity formula, depends on host and vector parameters, including the vector intrinsic ability to replicate then transmit the pathogen known as vector competence. Vec...Epidemiology, Vectors, VirusesSara Moutailler2023-06-17 15:59:17 View
23 Mar 2023
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The helper strategy in vector-transmission of plant viruses

The intriguing success of helper components in vector-transmission of plant viruses.

Recommended by based on reviews by Jamie Bojko and Olivier Schumpp

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 helper strategy in vector-transmission of plant virusesDi Mattia Jérémy, Zeddam Jean Louis, Uzest Marilyne and Stéphane Blanc<p>An intriguing aspect of vector-transmission of plant viruses is the frequent involvement of a helper component (HC). HCs are virus-encoded non-structural proteins produced in infected plant cells that are mandatory for the transmission success....Evolution of hosts, infectious agents, or vectors, Interactions between hosts and infectious agents/vectors, Molecular biology of infections, Molecular genetics of hosts, infectious agents, or vectors, Plant diseases, Vectors, VirusesChristine Coustau2022-10-28 17:32:39 View
14 Nov 2022
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Ehrlichia ruminantium uses its transmembrane protein Ape to adhere to host bovine aortic endothelial cells

Adhesion process of Ehrlichia ruminantium to its host cell: the role of the protein ERGACDS01230 elucidated

Recommended by based on reviews by Rodolfo García-Contreras and Alejandro Cabezas-Cruz

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

*Ehrlichia ruminantium* uses its transmembrane protein Ape to adhere to host bovine aortic endothelial cellsValérie Pinarello, Elena Bencurova, Isabel Marcelino, Olivier Gros, Carinne Puech, Mangesh Bhide, Nathalie Vachiery, Damien F. Meyer<p><em>Ehrlichia ruminantium</em> is an obligate intracellular bacterium, transmitted by ticks of the genus <em>Amblyomma</em> and responsible for heartwater, a disease of domestic and wild ruminants. High genetic diversity of <em>E. ruminantium</...Interactions between hosts and infectious agents/vectors, Microbiology of infectionsThomas Pollet Rodolfo García-Contreras, Alejandro Cabezas-Cruz2021-10-14 16:54:54 View
29 Jan 2024
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Spring reproductive success influences autumnal malarial load in a passerine bird

Avian Plasmodium parasitaemia as an indicator of reproduction investment

Recommended by ORCID_LOGO based on reviews by Luz García-Longoria and 2 anonymous reviewers

Effects of the seasonal variations on within-host parasitaemia are still not well understood and potentially due to numerous factors, e.g. host and parasite species, host sex or age, or geographical regions. In this study, over three years in Switzerland, Pigeault et al. (2024) collected data on great tits reproductive outputs – laying date, clutch size, fledging success – to determine whether they were associated with avian Plasmodium parasitaemia before (winter), during (spring) and after (autumn) the breeding season. They focused on two lineages from two species: a highly generalist lineage Plasmodium relictum (lineage SGS1; Bensch et al. 2009) and a more specialized lineage Plasmodium homonucleophilum (lineage SW2). As previously found, they showed that parasitaemia level is low during the winter and then increase in spring (Applegate, 1970; Applegate 1971). Spring recurrences have been intensively studied but are still not well understood since many non-exclusive factors can provoke them, i.e environmental stressors, reproductive hormones, co-infections or bites of mosquitoes (Cornet et al. 2014).

Interestingly, the parasitaemia level during the winter before and during the breeding season were not associated to the reproductive success, meaning that birds in their populations with low parasitaemia during the winter had not more fledglings than the ones with a higher parasitaemia. However, the individuals who invested the most in the reproduction with a higher number of fledglings had also a higher parasitaemia in the following autumn. The number of laid eggs was not associated with the parasitaemia during the following autumn, showing that the initial investment in the reproduction is less important than the parental care (e.g. chicks feeding) in terms of mid/long term cost. The originality here is that authors followed populations during three periods of the year, which is not an easy task and rarely done in natural populations. Their results highlight the mid/long-term effect of higher resource allocation into reproduction on individuals’ immune system and ability to control parasite replication. Further analyses on various lineages and bird populations from other geographical regions (i.e. different latitudes) would be the next relevant step.

References

Applegate JE (1971) Spring relapse of Plasmodium relictum infections in an experimental field population of English sparrows (Passer domesticus). Journal of Wildlife Diseases, 7, 37–42. https://doi.org/10.7589/0090-3558-7.1.37

Applegate JE, Beaudoin RL (1970) Mechanism of spring relapse in avian malaria: Effect of gonadotropin and corticosterone. Journal of Wildlife Diseases, 6, 443–447. https://doi.org/10.7589/0090-3558-6.4.443

Bensch S, Hellgren O, Pérez‐Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353-1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

Cornet S, Nicot A, Rivero A, Gandon S (2014) Evolution of plastic transmission strategies in avian malaria. PLoS Pathogens, 10, e1004308. https://doi.org/10.1371/journal.ppat.1004308

Pigeault R, Cozzarolo CS, Wassef J, Gremion J, Bastardot M, Glaizot O, Christe P (2024) Spring reproductive success influences autumnal malarial load in a passerine bird. bioRxiv ver 3. Peer reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.07.28.550923

Spring reproductive success influences autumnal malarial load in a passerine birdRomain Pigeault, Camille-Sophie Cozzarolo, Jérôme Wassef, Jérémy Gremion, Marc Bastardot, Olivier Glaizot, Philippe Christe<p>Although avian haemosporidian parasites are widely used as model organisms to study fundamental questions in evolutionary and behavorial ecology of host-parasite interactions, some of their basic characteristics, such as seasonal variations in ...Interactions between hosts and infectious agents/vectors, ParasitesClaire Loiseau Carolina Chagas, Anonymous, Luz García-Longoria2023-08-11 14:14:56 View
28 Sep 2023
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Influence of endosymbionts on the reproductive fitness of the tick Ornithodoros moubata

The cost of endosymbionts on the reproductive fitness of the soft tick Ornithodoros moubata

Recommended by ORCID_LOGO based on reviews by Luciana Raggi Hoyos and Tuomas Aivelo

Ticks are amongst the most important pathogen vectors in medical and veterinary clinical settings worldwide (Dantas-Torres et al., 2012). Like other holobionts, ticks live in association with a diverse microbiota. It includes tick-borne pathogens (TBP) and other microorganisms that have a beneficial or detrimental effect on the physiology of the host and can also affect the transmission of TBP to animals or humans. In this microbiota, primary endosymbionts, which are obligatory and inheritable, play a role in tick reproduction, the host defense and adaptation to varying environmental conditions (Duron et al., 2018). However, the effect of the microbiota structure and of the endosymbionts on tick fitness and reproduction is not well known. The soft tick Ornithodoros moubata, a parasite known to transmit African swine fever virus (Vial, 2009), is known to host Francisella-like and Rickettsia endosymbionts (Duron et al., 2018). These endosymbionts carry genes involved in B vitamin synthesis which may be supplemented to the host (Bonnet & Pollet, 2021). 

Here, the authors investigated the role of endosymbionts on the reproductive fitness of Ornithodoros moubata by conducting two experiments (Taraveau et al., 2023). First, they tested the effect of antibiotic treatment of 366 first-stage nymphs on the main endosymbionts Francisella-like and Rickettsia, and measured the endosymbionts presence overtime by qPCR. Second, they surveyed the effect of antibiotic treatment with or without the addition of B vitamins on the survival and reproductive fitness of 132 females over 50 days. This second experiment intended to identify whether the endosymbionts have an effect on the host reproduction or on its nutrition. The supplementation of B vitamin did not have a drastic effect on tick fitness or reproductive traits. However, antibiotic treatments reduced the presence of endosymbionts while increasing tick survival, suggesting a potential cost of hosting endosymbionts on the tick fitness.

The authors did a lot of work to thoroughly follow the propositions from Dr Raggi, Dr Aivelo and myself to reconstruct and to revise the manuscript. I believe that the manuscript now reads very well and the answers to the reviews also add some value to the manuscript. As Dr Aivelo pointed out, “this study follows the traditional path of so-called population perturbation studies, where ecologists have administered antibiotics or antihelminths to different animals and seen how the community changes and what effects this has on the host fitness and survival”. As both reviewers stated, results from this study are valuable and provide important basic knowledge that will likely help conduct future experiments on tick microbiota. This recommendation is the result of the thorough reviewing work of Dr Aivelo and Dr Raggi which I warmly thank.
 
References

Bonnet, S. I., & Pollet, T. (2021). Update on the intricate tango between tick microbiomes and tick‐borne pathogens. Parasite Immunology, 43(5), e12813. https://doi.org/10.1111/pim.12813

Dantas-Torres, F., Chomel, B. B., & Otranto, D. (2012). Ticks and tick-borne diseases: A One Health perspective. Trends in Parasitology, 28(10), 437–446. https://doi.org/10.1016/j.pt.2012.07.003

Duron, O., Morel, O., Noël, V., Buysse, M., Binetruy, F., Lancelot, R., Loire, E., Ménard, C., Bouchez, O., Vavre, F., & Vial, L. (2018). Tick-Bacteria Mutualism Depends on B Vitamin Synthesis Pathways. Current Biology, 28(12), 1896-1902.e5. https://doi.org/10.1016/j.cub.2018.04.038

Taraveau, F., Pollet, T., Duhayon, M., Gardès, L., & Jourdan-Pineau, H. (2023). Influence of endosymbionts on the reproductive fitness of the tick Ornithodoros moubata. bioRxiv, ver.3, peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.05.09.539061

Vial, L. (2009). Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite, 16(3), 191–202. https://doi.org/10.1051/parasite/2009163191

Influence of endosymbionts on the reproductive fitness of the tick *Ornithodoros moubata*Taraveau Florian, Pollet Thomas, Duhayon Maxime, Gardès Laëtitia, Jourdan-Pineau Hélène<p style="text-align: justify;">Over the past decade, many studies have demonstrated the crucial role of the tick microbiome in tick biology. The soft tick <em>Ornithodoros moubata</em> is a hematophagous ectoparasite of <em>Suidae</em>, best know...Mutualistic symbionts, Parasites, Pathogenic/Symbiotic Bacteria, Physiology of hosts, infectious agents, or vectors, VectorsAngélique Gobet2023-05-25 19:00:33 View