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07 Feb 2023
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Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populations

Unveiling the complex interactions between members of gut microbiomes: a significant advance provided by an exhaustive study of wild bank voles

Recommended by based on reviews by Jason Anders and 1 anonymous reviewer

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

Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populationsMarie Bouilloud, Maxime Galan, Adelaide Dubois, Christophe Diagne, Philippe Marianneau, Benjamin Roche, Nathalie Charbonnel<p>Background</p> <p>Despite its central role in host fitness, the gut microbiota may differ greatly between individuals. This variability is often mediated by environmental or host factors such as diet, genetics, and infections. Recently, a part...Disease Ecology/Evolution, Ecohealth, Interactions between hosts and infectious agents/vectors, Reservoirs, ZoonosesThomas Pollet2022-05-25 10:13:23 View
19 Jul 2023
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A soft tick vector of Babesia sp. YLG in Yellow-legged gull (Larus michahellis) nests

A four-year study reveals the potential role of the soft tick Ornithodoros maritimus in the transmission and circulation of Babesia sp. YLG in Yellow-legged gull colonies.

Recommended by based on reviews by Hélène Jourdan and Tahar Kernif

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
A soft tick vector of *Babesia* sp. YLG in Yellow-legged gull (*Larus michahellis*) nestsClaire Bonsergent, Marion Vittecoq, Carole Leray, Maggy Jouglin, Marie Buysse, Karen D. McCoy, Laurence Malandrin<p style="text-align: justify;"><em>Babesia </em>sp. YLG has recently been described in Yellow-legged gull (<em>Larus michahellis</em>) chicks and belongs to the Peircei clade in the new classification of Piroplasms. Here, we studied <em>Babesia <...Ecology of hosts, infectious agents, or vectors, Eukaryotic pathogens/symbionts, Interactions between hosts and infectious agents/vectors, Parasites, VectorsThomas Pollet2023-03-29 14:33:40 View
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 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
28 Oct 2022
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Development of nine microsatellite loci for Trypanosoma lewisi, a potential human pathogen in Western Africa and South-East Asia, and preliminary population genetics analyses

Preliminary population genetic analysis of Trypanosoma lewisi

Recommended by based on reviews by Gabriele Schönian and 1 anonymous reviewer

Trypanosoma lewisi is an atypical trypanosome species. Transmitted by fleas, it has a high prevalence and worldwide distribution in small mammals, especially rats [1]. Although not typically thought to infect humans, there has been a number of reports of human infections by T. lewisi in Asia including a case of a fatal infection in an infant [2]. The fact that the parasite is resistant to lysis by normal human serum [3] suggests that many people, especially immunocompromised individuals, may be at risk from zoonotic infections by this pathogen, particularly in regions where there is close contact with T. lewisi-infected rat fleas. Indeed, it is also possible that cryptic T. lewisi infections exist but have hitherto gone undetected. Such asymptomatic infections have been detected for a number of parasitic infections including the related parasite T. b. gambiense [4]. 
 
Despite the fact that T. lewisi parasites pose a risk to human health, very little is known about their population structure, reproductive mode, population size or dispersal. In the article [5], Ségard et al. presented the first attempt at examining the population structure of the parasite. They developed microsatellite markers and used them to analyse a small set of samples from West Africa and Southeast Asia. Although the number of microsatellite markers is not very high and they encountered problems of PCR amplification especially of the southeast Asian samples, they did provide preliminary data that hints at a clonal population structure with rare recombination and suggests population subdivisions occurring at a scale that is equal, and probably smaller than a neighborhood of several houses with a short generation time. These are very interesting preliminary findings that will need to be validated using a larger cohort with more markers or by whole genome sequencing.
 

References


[1] Hoare CA (1972) The trypanosomes of mammals. A zoological monograph. The trypanosomes of mammals. A zoological monograph.

[2] Truc P, Büscher P, Cuny G, Gonzatti MI, Jannin J, Joshi P, Juyal P, Lun Z-R, Mattioli R, Pays E, Simarro PP, Teixeira MMG, Touratier L, Vincendeau P, Desquesnes M (2013) Atypical Human Infections by Animal Trypanosomes. PLOS Neglected Tropical Diseases, 7, e2256. https://doi.org/10.1371/journal.pntd.0002256

[3] Lun Z-R, Wen Y-Z, Uzureau P, Lecordier L, Lai D-H, Lan Y-G, Desquesnes M, Geng G-Q, Yang T-B, Zhou W-L, Jannin JG, Simarro PP, Truc P, Vincendeau P, Pays E (2015) Resistance to normal human serum reveals Trypanosoma lewisi as an underestimated human pathogen. Molecular and Biochemical Parasitology, 199, 58–61. https://doi.org/10.1016/j.molbiopara.2015.03.007

[4] Büscher P, Bart J-M, Boelaert M, Bucheton B, Cecchi G, Chitnis N, Courtin D, Figueiredo LM, Franco J-R, Grébaut P, Hasker E, Ilboudo H, Jamonneau V, Koffi M, Lejon V, MacLeod A, Masumu J, Matovu E, Mattioli R, Noyes H, Picado A, Rock KS, Rotureau B, Simo G, Thévenon S, Trindade S, Truc P, Reet NV (2018) Do Cryptic Reservoirs Threaten Gambiense-Sleeping Sickness Elimination? Trends in Parasitology, 34, 197–207. https://doi.org/10.1016/j.pt.2017.11.008

[5] Ségard A, Roméro A, Ravel S, Truc P, Gauthier D, Gauthier P, Dossou H-J, Sylvestre B, Houéménou G, Morand S, Chaisiri K, Noûs C, De Meeûs T (2022) Development of nine microsatellite loci for Trypanosoma lewisi, a potential human pathogen in Western Africa and South-East Asia, and preliminary population genetics analyses. Zenodo, 6460010, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6460010

Development of nine microsatellite loci for Trypanosoma lewisi, a potential human pathogen in Western Africa and South-East Asia, and preliminary population genetics analysesAdeline Ségard, Audrey Romero, Sophie Ravel, Philippe Truc, Gauthier Dobigny, Philippe Gauthier, Jonas Etougbetche, Henri-Joel Dossou, Sylvestre Badou, Gualbert Houéménou, Serge Morand, Kittipong Chaisiri, Camille Noûs, Thierry deMeeûs<p><em>Trypanosoma lewisi</em> belongs to the so-called atypical trypanosomes that occasionally affect humans. It shares the same hosts and flea vector of other medically relevant pathogenic agents as Yersinia pestis, the agent of plague. Increasi...Animal diseases, Disease Ecology/Evolution, Ecology of hosts, infectious agents, or vectors, Eukaryotic pathogens/symbionts, Evolution of hosts, infectious agents, or vectors, Microbiology of infections, Parasites, Population genetics of hosts, in...Annette MacLeod2022-04-21 17:04:37 View
03 Nov 2023
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Longitudinal Survey of Astrovirus infection in different bat species in Zimbabwe: Evidence of high genetic Astrovirus diversity

High diversity and evidence for inter-species transmission in astroviruses surveyed from bats in Zibabwae

Recommended by based on reviews by 2 anonymous reviewers

Most infectious diseases of humans are zoonoses, and many of these come from particularly species diverse reservoir taxa, such as bats, birds, and rodents (1). Because of our changing landscape, there is increased exposure of humans to wildlife diseases reservoirs, yet we have little basic information about prevalence, hotspots, and transmission factors of most zoonotic pathogens. Viruses are particularly worrisome as a public health risk due to their fast mutation rates and well-known cross-species transmission abilities. There is a global push to better survey wildlife for viruses (2), but these studies are difficult, and the problem is vast. Astroviruses (AstVs) comprise a diverse family of ssRNA viruses known from mammals and birds. Astroviruses can cause gastroenteritis in humans and are more common in elderly and young children, but the relationship of human to non-human Astroviridae as well as transmission routes are unclear.  AstVs have been detected at high prevalence in bats in multiple studies (3,4), but it is unclear what factors, such as co-infecting viruses and bat reproductive phenology, influence viral shedding and prevalence.
In this recommended study, Vimbiso et al. (5) study the prevalence and diversity of astroviruses in different insectivorous and frugivorous chiropteran species roosting in trees, caves and building basements across Zimbabwe, a region never investigated for astroviruses. Using both pooled population samples and individual samples from 11 different sites, the authors screened for astrovirus prevalence via RT-PCR and identified bat taxa using mitochondrial gene sequencing. An overall prevalence of 10-14% infection was recorded. No clear association of increased astrovirus and coronavirus coinfection was detected, and although astrovirus infection varied over the season, it did not do so in consistent ways across the two primary sampling sites, Magweto and Chirundu. A phylogeny generated by sequencing all of the astrovirus positive samples showed evidence that most of the viral lineages are transmitting within species but across Zibabwae such that most phylogenetic lineages grouped viruses from the same host species together. However, there was ample evidence for interspecies transmission between bats. Finally, a small percentage of the total astrovirus diversity from Zibabwae clustered with sequences from humans. The timing and direction of the transmission between humans and bats need further investigation.
 
This study provides important baseline data about viral diversity and does an excellent job of capturing the spatial, temporal, host species, and sequence level dynamics of the astroviruses. There are clear limitations on how this study can be interpreted due to different sampling regimes and, in particular, the fact that each of the two primary sites was only explored for temporal variation over a single calendar year. That said, the grand diversity of astroviruses demonstrated in insectivorous bats in Zibabwae shows that we are only seeing the very tip of the iceberg with respect to viral diversity with zoonotic potential. As suggested by the reviewers, more studies like this are needed to understand the basic ecology of viruses and to aid in predicting epidemics.

References

1. Mollentze N, Streicker DG. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proceedings of the National Academy of Sciences. 2020 Apr 28;117(17):9423-30. https://doi.org/10.1073/pnas.1919176117
2. Carroll D, Daszak P, Wolfe ND, Gao GF, Morel CM, Morzaria S, et al. The Global Virome Project. Science. 2018 Feb 23;359(6378):872-4. https://doi.org/10.1126/science.aap7463
3. Lee SY, Son KD, Yong-Sik K, Wang SJ, Kim YK, Jheong WH, et al. Genetic diversity and phylogenetic analysis of newly discovered bat astroviruses in Korea. Arch Virol. 2018;163(11):3065-72. https://doi.org/10.1007/s00705-018-3992-6
4. Seltmann A, Corman VM, Rasche A, Drosten C, Czirják GÁ, Bernard H, et al. Seasonal Fluctuations of Astrovirus, But Not Coronavirus Shedding in Bats Inhabiting Human-Modified Tropical Forests. EcoHealth. 2017 Jun 1;14(2):272-84. https://doi.org/10.1007/s10393-017-1245-x
5. Vimbiso C, Hélène DN, Malika A, Getrude M, Valérie P, Ngoni C, et al. Longitudinal Survey of Astrovirus infection in different bat species in Zimbabwe: Evidence of high genetic Astrovirus diversity. bioRxiv, 2023.04.14.536987, ver. 6 peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.04.14.536987

Longitudinal Survey of Astrovirus infection in different bat species in Zimbabwe: Evidence of high genetic Astrovirus diversityVimbiso Chidoti, Helene De Nys, Malika Abdi, Getrudre Mashura, Valerie Pinarello, Ngoni Chiweshe, Gift Matope, Laure Guerrini, Davies Pfulenyi, Julien Cappelle, Ellen Mwandiringana, Dorothee Misse, Gori Elizabeth, Mathieu Bourgarel, Florian Liegeois<p>Astroviruses (AstVs) have been discovered in over 80 animal species including diverse bat species and avian species. A study on Astrovirus circulation and diversity in different insectivorous and frugivorous chiropteran species roosting in tree...Animal diseases, Epidemiology, Molecular genetics of hosts, infectious agents, or vectors, Reservoirs, Viruses, ZoonosesTim James2023-04-18 14:58:43 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
21 Jul 2022
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Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)

Understanding the in vitro evolution of Cyprinid herpesvirus 3 (CyHV-3), a story of structural variations that can lead to the design of attenuated virus vaccines

Recommended by based on reviews by Lucie Cappuccio and Veronique Hourdel

Structural variations (SVs) play a key role in viral evolution, and therefore they are also important for infection dynamics. However, the contribution of structural variations to the evolution of double-stranded viruses is limited. This knowledge can help to understand the population dynamics and might be crucial for the future development of viral attenuated vaccines.

In this study, Fuandila et al (1) use the Cyprinid herpesvirus 3 (CyHV-3), commonly known as koi herpesvirus (KHV), to investigate the variability and contribution of structural variations (SV) for viral evolution after 99 passages in vitro. This virus, with the largest genome among herperviruses, causes a lethal infection in common carp and koi associated with mortalities up to 95% (2). Interestingly, KHV infections are caused by haplotype mixtures, which possibly are a source of genome diversification, but make genomic comparisons more difficult.

The authors have used ultra-deep long-read sequencing of two passages, P78 and P99, which were previously described to have differences in virulence. They have found a surprisingly high and wide distribution of SVs along the genome, which were enriched in inversion and deletion events and that often led to defective viral genomes. Although it is known that these defective viral genomes negatively impact viral replication, their implications for virus persistence are still unclear.

Subsequently, the authors concentrated on the virulence-relevant region ORF150, which was found to be different in P78 (deletion in 100% of the reads) and P99 (reference-like haplotype). To understand this loss and gain of full ORF150, they searched for SV turn-over in 10 intermediate passages. This analysis revealed that by passage 10 deleted and inverted (attenuated) haplotypes had already appeared, steadily increased frequency until P78, and then completely disappeared between P78 and P99. This is a striking result that raises new questions as to how this clearance occurs, which is really important as these reversions may result in undesirable increases in virulence of live-attenuated vaccines.

We recommend this preprint because its use of ultra-deep long-read sequencing has permitted to better understand the role of SV diversity and dynamics in viral evolution. This study shows an unexpectedly high number of structural variations, revealing a novel source of virus diversification and confirming the different mixtures of haplotypes in different passages, including the gain of function. This research provides basic knowledge for the future design of live-attenuated vaccines, to prevent the reversion to virulent viruses. 

References

(1)  Fuandila NN, Gosselin-Grenet A-S, Tilak M-K, Bergmann SM, Escoubas J-M, Klafack S, Lusiastuti AM, Yuhana M, Fiston-Lavier A-S, Avarre J-C, Cherif E (2022) Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV). bioRxiv, 2022.03.10.483410, ver. 4 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.03.10.483410

(2)  Sunarto A, McColl KA, Crane MStJ, Sumiati T, Hyatt AD, Barnes AC, Walker PJ. Isolation and characterization of koi herpesvirus (KHV) from Indonesia: identification of a new genetic lineage. Journal of Fish Diseases, 34, 87-101. https://doi.org/10.1111/j.1365-2761.2010.01216.x 

Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)Nurul Novelia Fuandila, Anne-Sophie Gosselin-Grenet, Marie-Ka Tilak, Sven M Bergmann, Jean-Michel Escoubas, Sandro Klafack, Angela Mariana Lusiastuti, Munti Yuhana, Anna-Sophie Fiston-Lavier, Jean-Christophe Avarre, Emira Cherif<p style="text-align: justify;">Structural variations (SVs) constitute a significant source of genetic variability in virus genomes. Yet knowledge about SV variability and contribution to the evolutionary process in large double-stranded (ds)DNA v...Animal diseases, Evolution of hosts, infectious agents, or vectors, Genomics, functional genomics of hosts, infectious agents, or vectors, VirusesJorge Amich Lucie Cappuccio, 2022-03-11 10:50:50 View
08 Aug 2023
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A global Corynebacterium diphtheriae genomic framework sheds light on current diphtheria reemergence

DIPHTOSCAN : A new tool for the genomic surveillance of diphtheria

Recommended by based on reviews by Ankur Mutreja and 2 anonymous reviewers

One of the greatest achievements of health sciences is the eradication of infectious diseases such as smallpox that in the past imposed a severe burden on humankind, through global vaccination campaigns. Moreover, progress towards the eradication of others such as poliomyelitis, dracunculiasis, and yaws is being made.

In contrast, other infections that were previously contained are reemerging, due to several factors, including lack of access to vaccines due to geopolitical reasons, the rise of anti-vaccine movements, and the constant mobility of infected persons from the endemic sites.

One of such disease is diphtheria, caused by Corynebacterium diphtheriae and a few other related species such as C. ulcerans and C. pseudotuberculosis. Importantly, in France, diphtheria cases reported in 2022 increased 7-fold from the average of previously recorded cases per year in the previous 4 years and the situation in other European countries is similar.

Hence, as reported here, Hennart et al. (2023) developed DIPHTOSCAN, a free access bioinformatics tool with user-friendly interphase, aimed to easily identify, extract and interpret important genomic features such as the sublineage of the strain, the presence of the tox gene (as a string predictor for toxigenic disease) as well as genes coding other virulence factors such as fimbriae, and the presence of know resistant mechanisms towards antibiotics like penicillin and erythromycin currently used in the clinic to treat this infection.

The authors validated the performance of their tool with a large collection of genomes, including those obtained from the isolates of the 2022 outbreak in France, more than 1,200 other genomes isolated from France, Algeria, and Yemen, and more than 500 genomes from several countries from Europe, America, Africa, Asia, and Oceania that are available through the NCBI site.

DIPHTOSCAN will allow the rapid identification and surveillance of potentially dangerous strains such as those being tox-positive isolates and resistant to multiple drugs and/or first-line treatments and a better understanding of the epidemiology and evolution of this important reemerging disease.

Reference

Hennart M., Crestani C., Bridel S., Armatys N., Brémont S., Carmi-Leroy A., Landier A., Passet V., Fonteneau L., Vaux S., Toubiana J., Badell E. and Brisse S. (2023). A global Corynebacterium diphtheriae genomic framework sheds light on current diphtheria reemergence. bioRxiv, 2023.02.20.529124, ver 3 peer-reviewed and recommended by PCI Infections. https://doi.org/10.1101/2023.02.20.529124

A global *Corynebacterium diphtheriae* genomic framework sheds light on current diphtheria reemergenceMelanie Hennart, Chiara Crestani, Sebastien Bridel, Nathalie Armatys, Sylvie Brémont, Annick Carmi-Leroy, Annie Landier, Virginie Passet, Laure Fonteneau, Sophie Vaux, Julie Toubiana, Edgar Badell, Sylvain Brisse<p style="text-align: justify;"><strong>Background</strong></p> <p style="text-align: justify;">Diphtheria, caused by <em>Corynebacterium diphtheriae</em>, reemerges in Europe since 2022. Genomic sequencing can inform on transmission routes and g...Drug resistance, tolerance and persistence, Epidemiology, Evolution of hosts, infectious agents, or vectors, Genomics, functional genomics of hosts, infectious agents, or vectors, Microbiology of infections, Population genetics of hosts, infectiou...Rodolfo García-Contreras Ankur Mutreja 2023-03-09 16:02:27 View
14 Dec 2022
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Transcriptome responses of the aphid vector Myzus persicae are shaped by identities of the host plant and the virus

How do multiple host plants and virus species challenge aphid molecular machinery?

Recommended by based on reviews by Juan José Lopez Moya and Michelle Heck

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

Transcriptome responses of the aphid vector *Myzus persicae* are shaped by identities of the host plant and the virusQuentin Chesnais, Victor Golyaev, Amandine Velt, Camille Rustenholz, Maxime Verdier, Véronique Brault, Mikhail M. Pooggin, Martin Drucker<p style="text-align: justify;"><strong>Background:</strong> Numerous studies have documented modifications in vector orientation behavior, settling and feeding behavior, and/or fecundity and survival due to virus infection in host plants. These a...Behaviour of hosts, infectious agents, or vectors, Cell biology of hosts, infectious agents, or vectors, Molecular biology of infections, Physiology of hosts, infectious agents, or vectors, Phytopathology, Plant diseases, Vectors, VirusesSebastien Massart2022-07-19 15:24:14 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