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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
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
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
23 Jan 2023
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Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense

Whole genome transcriptome reveals metabolic and immune susceptibility factors for Trypanosoma congolense infection in West-African livestock

Recommended by based on reviews by 2 anonymous reviewers

African trypanosomiasis is caused by to the infection of a protozoan parasite of the Trypanosoma genus. It is transmitted by the tsetse fly, and is largely affecting cattle in the sub-humid areas of Africa, causing a high economic impact. However, not all the bovine strains are equally susceptible to the infection (1). 

In order to dissect the mechanisms underlying susceptibility to African trypanosoma infection, Peylhard et al (2) performed blood transcriptional profiles of trypanotolerant, trypanosensitive and mixed cattle breeds, before and after experimental infection with T. congolense

First of all, the authors have characterized the basal transcriptional profiles in the blood of the different breeds under study, which could be classified in a wide array of functional pathways. Of note, after infection some pathways were consistently enriched in all the group tested. Among them, the immune system-related ones were again on the top functions reported. The search for specific canonical pathways pointed to a prominent role of lipid and cholesterol-related pathways, as well as mitochondrial function and B and T lymphocyte activation.

However, the analysis of infected animals demonstrated that trypanosusceptible animals showed a stronger transcriptomic reprogramming, highly enriched in specific metabolic and immunological pathways. It is worthy to highlight striking differences in genes involved in immune signal transduction, cytokines and markers of different leukocyte subpopulations.

This work represents undoubtedly a significant momentum in the field, since the authors explore in deep a wide panel of cattle breeds representing the majority of West-African taurine and zebu in a systematic way. Since the animals were studied at different timepoints after infection, future longitudinal analyses of these datasets will be providing a precious insight on the kinetics of immune and metabolic reprogramming associated with susceptibility and tolerance to African trypanosoma infection, widening the application of this interesting study into new therapeutic interventions.

References

1. Berthier D, Peylhard M, Dayo G-K, Flori L, Sylla S, Bolly S, Sakande H, Chantal I, Thevenon S (2015) A Comparison of Phenotypic Traits Related to Trypanotolerance in Five West African Cattle Breeds Highlights the Value of Shorthorn Taurine Breeds. PLOS ONE, 10, e0126498. https://doi.org/10.1371/journal.pone.0126498

2. Peylhard M, Berthier D, Dayo G-K, Chantal I, Sylla S, Nidelet S, Dubois E, Martin G, Sempéré G, Flori L, Thévenon S (2022) Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense. bioRxiv, 2022.06.10.495622, ver. 2 peer-reviewed and recommended by Peer Community Infections. https://doi.org/10.1101/2022.06.10.495622.

Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolenseMoana Peylhard, David Berthier, Guiguigbaza-Kossigan Dayo, Isabelle Chantal, Souleymane Sylla, Sabine Nidelet, Emeric Dubois, Guillaume Martin, Guilhem Sempéré, Laurence Flori, Sophie Thévenon<p>Animal African trypanosomosis, caused by blood protozoan parasites transmitted mainly by tsetse flies, represents a major constraint for millions of cattle in sub-Saharan Africa. Exposed cattle include trypanosusceptible indicine breeds, severe...Animal diseases, Genomics, functional genomics of hosts, infectious agents, or vectors, Resistance/Virulence/ToleranceConcepción MarañónAnonymous, Anonymous2022-06-14 17:06:57 View
08 Dec 2022
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Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystems

Zoonotic emergence and the overlooked case of cities

Recommended by based on reviews by Eric Dumonteil, Nicole L. Gottdenker and 1 anonymous reviewer

Zoonotic pathogens, those transmitted from animals to humans, constitute a major public health risk with high associated global economic costs. Diseases associated with these pathogens represent more than 60% of emerging infectious diseases and predominantly originate in wildlife (1). Over the last decades, the emergence and re-emergence of zoonotic pathogens have led to an increasing number of epidemics, as illustrated by the current Covid-19 pandemic. There is ample evidence that human impact on native ecosystems such as deforestation, agricultural development, and urbanization, is linked to spillover of pathogens from animals to humans (2). However, research and calls to action have mainly focused on the importance of surveillance and prevention of zoonotic emergences along landscape interfaces, with special emphasis on tropical forests and agroecosystems, and studies and reviews pointing out the zoonotic risk associated with cities are scarce.  Additionally, cities are sometimes wrongly seen as one homogeneous ecosystem, almost exclusively human, with a Northern hemisphere-biased perception of what a city is, which fails to take into account the ecological and socio-economic diversities that can constitute an urban area.

Here, Dobigny and Morand (3) aim to draw attention to the importance of urban ecosystems in zoonotic risk and advocate that further attention should be paid to urban, peri-urban and suburban areas. In this well-organized and well-documented review, the authors show, using updated literature, that cities are places where massive contacts occur between wildlife, domestic animals, and human inhabitants (thus constituting spillover opportunities), and that it is even likely that human and wildlife contact in urban centers is more prevalent than in wild areas, perhaps contrary to intuition. Indeed, cities currently constitute the most important environment of human life and are places for millions of close interactions between humans and animals, including pets and domestic animals, wild animals through the intrusion of wild urban-adapted species (e.g., some bat, rodent, or bird species among others), manipulation and consumption of wildlife meat, and the existence of wildlife meat markets, which all constitute a major risk for zoonotic spillover. In cities, lab escapees of zoonotic pathogens also exist, and trends of adaptation to urban ecological conditions of many vectors of primary health importance is also a concern. The authors further argue that cities are predominant places for both epidemic amplification of human-human transmitted pathogens, because they are places with high human densities and population growth, and for dissemination of reservoirs, vectors and pathogens, as they are transport hubs. Dobigny & Morand further predict, likely correctly, that cities may be important places for pathogen evolution.  Finally, they propose actions and recommendations to limit the risk of zoonotic spillover events from urban ecosystems and future directions for research aiming at assessing this risk. 

The reviewers found the manuscript well-organized and presented, timely, and bringing novel contributions to the field of zoonotic emergence. I strongly recommend this article, which should benefit a large audience, particularly in the context of the current Covid-19 pandemics and the ongoing One Health initiatives aiming at preventing future zoonotic disease emergence (4). 

References

(1) Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature, 451, 990–993. https://doi.org/10.1038/nature06536

(2) White RJ, Razgour O (2020) Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review, 50, 336–352. https://doi.org/10.1111/mam.12201

(3) Dobigny G, Morand S (2022) Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystems. Zenodo, 6444776, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6444776

(4) Morand S, Lajaunie C (2021) Biodiversity and COVID-19: A report and a long road ahead to avoid another pandemic. One Earth, 4, 920–923. https://doi.org/10.1016/j.oneear.2021.06.007

Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystemsDobigny, G. & Morand, S.<p style="text-align: justify;">Zoonotic emergence requires spillover from animals to humans, hence animal-human interactions. A lot has been emphasized on human intrusion into wild habitats (e.g., deforestation, hunting) and the development of ag...Disease Ecology/Evolution, Ecohealth, Ecology of hosts, infectious agents, or vectors, Evolution of hosts, infectious agents, or vectors, One Health, ZoonosesEtienne Waleckx2022-04-11 11:39:11 View