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14 Feb 2024
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A Bayesian analysis of birth pulse effects on the probability of detecting Ebola virus in fruit bats

Epidemiological modeling to optimize the detection of zoonotic viruses in wild (reservoir) species

Recommended by ORCID_LOGO based on reviews by Hetsron Legrace NYANDJO BAMEN and 1 anonymous reviewer

Various species of Ebolavirus have caused, and are still causing, zoonotic outbreaks and public health crises in Africa. Bats have long been hypothesized to be important reservoir populations for a series of viruses such as Hendra or Marburg viruses, the severe acute respiratory syndrome coronavirus (SARS-CoV, SARS-CoV-2) as well as Ebolaviruses [2, 3]. However the ecology of disease dynamics, disease transmission, and coevolution with their natural hosts of these viruses is still poorly understood, despite their importance for predicting novel outbreaks in human or livestock populations. The evidence that bats function as sylvatic reservoirs for Ebola viruses is yet only partial. Indeed, only few serological studies demonstrated the presence of Ebolavirus antibodies in young bats [4], albeit without providing positive controls of viral detection or identifying the viral species (via PCR). There is thus an unexplained discrepancy between serological data and viral detection [2, 4]. 

In this article, Pleydell et al. [1] use a modeling approach as well as published serological and age-structure (of the bat population) data to calibrate the model simulations. The study starts with the development of an age-structured epidemiological model which includes seasonal birth pulses and waning immunity, both generating pulses of Ebolavirus transmission within a colony of African straw-coloured fruit bats (Eidolon helvum). The epidemiological dynamics of such system of ordinary differential equations can generate annual outbreaks, skipped years or multi-annual cycles up to chaotic dynamics. Therefore, the calibration of the parameters, and the definition of biologically relevant priors, are key. To this aim, the serological data are obtained from a previous study in Cameroon [5], and the age structured of the bat population (birth and mortality) from a population study in Ghana [6]. These data are integrated into the Bayesian analysis and statistical framework to fit the model and generate predictions. In a nutshell, the authors show an overlap between the data and credibility intervals generated by the calibrated model, which thus explains well the seasonality of age-structure, namely changes in pup presence, number of lactating females, or proportion of juveniles in May. The authors can estimate that 76% of adults and 39% of young bats do survive each year, and infections are expected to last one and a half weeks. The epidemiological model predicts that annual birth pulses likely generate annual disease outbreaks, so that weeks 30 to 31 of each year, are predicted to be the best period to isolate the circulating Ebolavirus in this bat population. From the model predictions, the authors estimate the probability to have missed an infectious bat among all the samples tested by PCR being approximately of one per two thousands. The disease dynamics pattern observed in the serology data, and replicated by the model, is likely driven by seasonal pulses of young susceptible bats entering the population. This seasonal birth event increases the viral transmission, resulting in the observed peak of viral prevalence. With the inclusion of immunity waning and antibody persistence, the model results illuminate therefore why previous studies have detected only few positive cases by PCR tests, in contrast to the evidence from serological data. 

 This study provides a first proof of principle that epidemiological modeling, despite its many simplifying assumptions, can be applied to wild species reservoirs of zoonotic diseases in order to optimize the design of field studies to detect viruses. Furthermore, such models can contribute to assess the probability and timing of zoonotic outbreaks in human or livestock populations. This article illustrates one of the manifold applications of mathematical theory of disease epidemiology to optimize sampling of pathogens/parasites or vaccine development and release [7, 8]. The further coupling of such models with population genetics theory and statistical inference methods (using parasite genome data) increasingly provide insights into the adaptation and evolution of parasites to human, crops and livestock populations [9, 10].

 

References

[1] Pleydell D.R.J., Ndong Bass I., Mba Djondzo F.A., Djomsi D.M., Kouanfack C., Peeters M., and J. Cappelle. 2023. A Bayesian analysis of birth pulse effects on the probability of detecting Ebola virus in fruit bats. bioRxiv, ver. 3 peer reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.08.10.552777

[2] Caron A., Bourgarel M., Cappelle J., Liégeois F., De Nys H.M., and F. Roger. 2018. Ebola virus maintenance: if not (only) bats, what else? Viruses 10, 549. https://doi.org/10.3390/v10100549

[3] Letko M., Seifert S.N., Olival K.J., Plowright R.K., and V.J. Munster. 2020. Bat-borne virus diversity, spillover and emergence. Nature Reviews Microbiology 18, 461–471. https://doi.org/10.1038/s41579-020-0394-z

[4] Leroy E.M., Kumulungui B., Pourrut X., Rouquet P., Hassanin A., Yaba P., Délicat A., Paweska J.T., Gonzalez J.P., and R. Swanepoel. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438, 575–576. https://doi.org/10.1038/438575a

[5] Djomsi D.M. et al. 2022. Dynamics of antibodies to Ebolaviruses in an Eidolon helvum bat colony in Cameroon. Viruses 14, 560. https://doi.org/10.3390/v14030560

[6] Peel A.J. et al. 2016. Bat trait, genetic and pathogen data from large-scale investigations of African fruit bats Eidolon helvum. Scientific data 3, 1–11. https://doi.org/10.1038/sdata.2016.49

[7] Nyandjo Bamen H.L., Ntaganda J.M., Tellier A. and O. Menoukeu Pamen. 2023. Impact of imperfect vaccine, vaccine trade-off and population turnover on infectious disease dynamics. Mathematics, 11(5), p.1240. https://doi.org/10.3390/math11051240

[8] Saadi N., Chi Y.L., Ghosh S., Eggo R.M., McCarthy C.V., Quaife M., Dawa J., Jit M. and A. Vassall. 2021. Models of COVID-19 vaccine prioritisation: a systematic literature search and narrative review. BMC medicine, 19, pp.1-11. https://doi.org/10.1186/s12916-021-02190-3

[9] Maerkle, H., John S., Metzger, L., STOP-HCV Consortium, Ansari, M.A., Pedergnana, V. and Tellier, A., 2023. Inference of host-pathogen interaction matrices from genome-wide polymorphism data. bioRxiv, https://doi.org/10.1101/2023.07.06.547816.

[10] Gandon S., Day T., Metcalf C.J.E. and B.T. Grenfell. 2016. Forecasting epidemiological and evolutionary dynamics of infectious diseases. Trends in ecology & evolution, 31(10), pp.776-788. https://doi.org/10.1016/j.tree.2016.07.010

A Bayesian analysis of birth pulse effects on the probability of detecting Ebola virus in fruit batsDavid R.J. Pleydell, Innocent Ndong Bass, Flaubert Auguste Mba Djondzo, Dowbiss Meta Djomsi, Charles Kouanfack, Martine Peeters, Julien Cappelle <p>Since 1976 various species of Ebolavirus have caused a series of zoonotic outbreaks and public health crises in Africa. Bats have long been hypothesised to function as important hosts for ebolavirus maintenance, however the transmission ecology...Animal diseases, Disease Ecology/Evolution, Ecohealth, Ecology of hosts, infectious agents, or vectors, Epidemiology, Population dynamics of hosts, infectious agents, or vectors, Reservoirs, Viruses, ZoonosesAurelien Tellier2023-08-16 16:57:05 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
07 Oct 2022
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Guidelines for the reliable use of high throughput sequencing technologies to detect plant pathogens and pests

High-throughput sequencing for the diagnostic of plant pathologies and identification of pests: recommendations and challenges

Recommended by based on reviews by Denise Altenbach and David Roquis

High-throughput sequencing (HTS) has revealed an incredible diversity of microorganisms in ecosystems and is also changing the monitoring of macroorganism biodiversity (Deiner et al. 2017; Piper et al. 2019).  

The diagnostic of plant pathogens and the identification of pests is gradually integrating the use of these techniques, but there are still obstacles. Most of them are related to the reliability of these analyses, which have long been considered insufficient because of their dependence on a succession of sophisticated operations involving parameters that are sometimes difficult to adapt to complex matrices or certain diagnostic contexts. The need to validate HTS approaches is gradually being highlighted in recent work but remains poorly documented (Bester et al. 2022).

In this paper, a large community of experts presents and discusses the key steps for optimal control of HTS performance and reliability in a diagnostic context (Massart et al. 2022). It also addresses the issue of costs. The article provides recommendations that closely combine the quality control requirements commonly used in conventional diagnostics with newer or HTS-specific control elements and concepts that are not yet widely used. It discusses the value of these for the use of the various techniques currently covered by the terms "High Throughput Sequencing" in diagnostic activities. The elements presented are intended to limit false positive or false negative results but will also optimise the interpretation of contentious results close to the limits of analytical sensitivity or unexpected results, both of which appear to be frequent when using HTS.

Furthermore, the need for risk analysis, verification and validation of methods is well illustrated with numerous examples for each of the steps considered crucial to ensure reliable use of HTS. The clear contextualisation of the proposals made by the authors complements and clarifies the need for user expertise according to the experimental objectives. Some unanswered questions that will require further development and validation are also presented.

This article should benefit a large audience including researchers with some level of expertise in HTS but unfamiliar with the recent concepts of controls common in the diagnostic world as well as scientists with strong diagnostic expertise but less at ease with the numerous and complex procedures associated with HTS.

References

Bester R, Steyn C, Breytenbach JHJ, de Bruyn R, Cook G, Maree HJ (2022) Reproducibility and Sensitivity of High-Throughput Sequencing (HTS)-Based Detection of Citrus Tristeza Virus and Three Citrus Viroids. Plants, 11, 1939. https://doi.org/10.3390/plants11151939

Deiner K, Bik HM, Mächler E, Seymour M, Lacoursière-Roussel A, Altermatt F, Creer S, Bista I, Lodge DM, de Vere N, Pfrender ME, Bernatchez L (2017) Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Molecular Ecology, 26, 5872–5895. https://doi.org/10.1111/mec.14350

Massart, S et al. (2022) Guidelines for the reliable use of high throughput sequencing technologies to detect plant pathogens and pests. Zenodo, 6637519, ver. 3  peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6637519

Piper AM, Batovska J, Cogan NOI, Weiss J, Cunningham JP, Rodoni BC, Blacket MJ (2019) Prospects and challenges of implementing DNA metabarcoding for high-throughput insect surveillance. GigaScience, 8, giz092. https://doi.org/10.1093/gigascience/giz092

Guidelines for the reliable use of high throughput sequencing technologies to detect plant pathogens and pestsS. Massart, I. Adams, M. Al Rwahnih, S. Baeyen, G. J. Bilodeau, A. G. Blouin, N. Boonham, T. Candresse, A. Chandelier, K. De Jonghe, A. Fox, Y.Z.A. Gaafar, P. Gentit, A. Haegeman, W. Ho, O. Hurtado-Gonzales, W. Jonkers, J. Kreuze, D. Kutjnak, B. B...<p style="text-align: justify;">High-throughput sequencing (HTS) technologies have the potential to become one of the most significant advances in molecular diagnostics. Their use by researchers to detect and characterize plant pathogens and pests...Diagnosis, Pest management, Phytopathology, Plant diseasesOlivier Schumpp2022-06-13 11:26:18 View
19 Feb 2024
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Population genetics of Glossina palpalis gambiensis in the sleeping sickness focus of Boffa (Guinea) before and after eight years of vector control: no effect of control despite a significant decrease of human exposure to the disease

Reaching the last miles for transmission interruption of sleeping sickness in Guinea: follow-up of achievements and policy making using microsatellites-based population genetics

Recommended by ORCID_LOGO based on reviews by Fabien HALKETT and 2 anonymous reviewers

Thanks to the coordinated and sustained efforts of national control programs, the World Health Organization (WHO), bilateral cooperation and nongovernmental organizations, the incidence of Human African Trypanosomiasis (HAT), better known as sleeping sickness, has drastically decreased during the last two decades (WHO, 2023a). Indeed, between 1999 and 2022, the reported number of new cases of the chronic form of sleeping sickness (Trypanosoma brucei gambiense) fell by 97% (from 27 862 to 799), and the number of newly reported cases of the acute form of HAT (Trypanosoma brucei rhodesiense) fell by 94% (from 619 to 38) (WHO, 2023b). These encouraging trends led the WHO to target this debilitating and highly fatal (if untreated) vector-borne parasitic disease for elimination as a public health problem by 2020, and for interruption of transmission (zero case) by 2030 (WHO, 2021, WHO, 2023a). However, the disease is persisting in many foci, and even some cases of resurgence have been documented after unfortunate events such as war or pandemics (Moore et al., 1999; Sah et al., 2023. Simarro et al). Although effective control measures, diagnosis and treatment are complex and require specific skills (WHO, 2023), especially in a context which animal reservoirs, including hidden reservoirs, can contribute to the maintenance/persistence of infection (Welburn and Maudlin, 2012; Camara et al., 2021). Vector control therefore appears as a viable alternative to accelerate sleeping sickness transmission interruption, and WHO has identified some critical actions for HAT elimination, including the coordination of vector control and animal trypanosomiasis management among countries, stakeholders and other sectors (e.g. tourism and wildlife) through multisectoral national bodies to maximize synergies (WHO, 2021).

The paper by Kagbadouno and Collaborators (2024) uses microsatellite markers genotyping and population genetics tools to investigate the impact of 11 years of tiny target-based vector control on the population biology of Glossina palpalis gambiensis in Boffa, one of the three active sleeping sickness foci in Guinea (Kagbadouno et al., 2012). Although vector control significantly reduced the apparent densities of tsetse flies (and therefore the human exposure to the vector) as well as the prevalence and incidence of the disease in the Boffa HAT focus (Courtin et al., 2015), no genetic signature of vector control was observed as no difference in population size, before and after the onset of the control policy, was found. The authors then provided national programs and implementing partners with indications on the actions to be taken to (i) maintain the achievements of vector control (thus avoiding rebound/resurgence as was experienced in the past (Franco et al., 2014), and (ii) accelerate the momentum towards elimination by for example combining these vector control efforts with medical surveys for case detection and treatment, in line with WHO recommendations (WHO, 2021). 

References

Camara M, Soumah AM, Ilboudo H, Travaillé C, Clucas C, Cooper A, Kuispond Swar NR, Camara O, Sadissou I, Calvo Alvarez E, Crouzols A, Bart JM, Jamonneau V, Camara M, MacLeod A, Bucheton B, Rotureau B. Extravascular Dermal Trypanosomes in Suspected and Confirmed Cases of gambiense Human African Trypanosomiasis. Clin Infect Dis. 2021 Jul 1;73(1):12-20. https://doi.org/10.1093/cid/ciaa897

Courtin F, Camara M, Rayaisse JB, Kagbadouno M, Dama E, Camara O, Traore IS, Rouamba J, Peylhard M, Somda MB, Leno M, Lehane MJ, Torr SJ, Solano P, Jamonneau V, Bucheton B (2015) Reducing human-tsetse contact significantly enhances the efficacy of sleeping sickness active screening campaigns: a promising result in the context of elimination. PLoS Neglected Tropical Diseases, 9. https://doi.org/10.1371/journal.pntd.0003727

Franco JR, Simarro PP, Diarra A, Jannin JG. (2014) Epidemiology of human African trypanosomiasis. Clin Epidemiol. 6:257-75. https://doi.org/10.2147/CLEP.S39728

Kagbadouno, M. S., Séré, M., Ségard, A., Camara, A. D., Camara, M., Bucheton, B., ... & Ravel, S. (2023). Population genetics of Glossina palpalis gambiensis in the sleeping sickness focus of Boffa (Guinea) before and after eight years of vector control: no effect of control despite a significant decrease of human exposure to the disease. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.07.25.550445

Kagbadouno MS, Camara M, Rouamba J, Rayaisse JB, Traoré IS, Camara O, Onikoyamou MF, Courtin F, Ravel S, De Meeûs T, Bucheton B, Jamonneau V, Solano P (2012) Epidemiology of sleeping sickness in boffa (Guinea): where are the trypanosomes? PLoS Neglected Tropical Diseases, 6, e1949. https://doi.org/10.1371/journal.pntd.0001949 

Moore A, Richer M, Enrile M, Losio E, Roberts J, Levy D. Resurgence of sleeping sickness in Tambura County, Sudan. Am J Trop Med Hyg. 1999 Aug;61(2):315-8. https://doi.org/10.4269/ajtmh.1999.61.315

Sah R, Mohanty A, Rohilla R, Padhi BK. A resurgence of Sleeping sickness amidst the COVID-19 pandemic: Correspondence. Int J Surg Open. 2023 Apr;53:100604. https://doi.org/10.1016/j.ijso.2023.100604

Welburn SC, Maudlin I. Priorities for the elimination of sleeping sickness. Adv Parasitol. 2012;79:299-337. https://doi.org/10.1016/B978-0-12-398457-9.00004-4

World Health Organization, 2021. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. World Health Organization, Geneva, Switzerland. ISBN: 978 92 4 001035 2. 196p. 

World Health Organization, 2023a. Trypanosomiasis, human African (sleeping sickness): key facts. Accessed at https://www.who.int/news-room/fact-sheets/detail/trypanosomiasis-human-african-(sleeping-sickness) on February 19, 2023.

World Health Organization, 2023b. Human African Trypanosomiasis, (sleeping sickness): the global health observatory. Accessed at https://www.who.int/data/gho/data/themes/topics/human-african-trypanosomiasis on February 19, 2023.

Population genetics of *Glossina palpalis* gambiensis in the sleeping sickness focus of Boffa (Guinea) before and after eight years of vector control: no effect of control despite a significant decrease of human exposure to the diseaseMoise S. Kagbadouno, Modou Séré, Adeline Ségard, Abdoulaye Dansy Camara, Mamadou Camara, Bruno Bucheton, Jean-Mathieu Bart, Fabrice Courtin, Thierry de Meeûs, Sophie Ravel<p style="text-align: justify;">Human African trypanosomosis (HAT), also known as sleeping sickness, is still a major concern in endemic countries. Its cyclical vector are biting insects of the genus Glossina or tsetse flies. In Guinea, the mangro...Disease Ecology/Evolution, Ecology of hosts, infectious agents, or vectors, Evolution of hosts, infectious agents, or vectors, Parasites, Population genetics of hosts, infectious agents, or vectorsHugues Nana Djeunga2023-07-29 13:24:52 View
27 Feb 2023
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African army ants at the forefront of virome surveillance in a remote tropical forest

A groundbreaking study using ants revealed a spectacular diversity of viruses in hardly accessible ecosystems like tropical forests

Recommended by based on reviews by Mart Krupovic and 1 anonymous reviewer

Deciphering the virome (the set or assemblage of viruses) of the Earth, from individual organisms to entire ecosystems, has become a key priority. The first step to better understanding the impact of viruses on the ecology and functions of ecosystems is to describe their diversity. Such knowledge opens the gates to a better assessment of global nutrient cycling or of the threat that viruses represent to individual health. This explains the increasing number of pioneering studies that are currently sequencing the complete or partial genome of thousands of new viruses [1].

In their exciting study, Fritz and collaborators [2], authors sampled 209 army ants (Genus Dorylus) to investigate the virus diversity in dense forests that researchers cannot easily access. Indeed, these ants live in colonies (21 were sampled) that can move 1 km per day, covering a significant area and attacking many invertebrate and vertebrate preys.  Each sample was sequenced by a protocol called VANA sequencing and allowing the enrichment of the sample in viral sequences [3], so improving the detection of viruses present at low abundance in the ant (and more specifically in its gut for viruses infecting preys). 

Around 45,000 contigs presented homologies with bacterial, plant, invertebrate, and vertebrate infecting viruses. Half could be assigned to 56 families and 157 genera of the International Committee on Taxonomy of Viruses. Beyond this amazing harvest of new and known virus sequences using an original methodology, the results significantly improve the current frontiers of known viral taxonomy and diversity and raise exciting research tracks to expand them. 

As a preprint, several blogs or news of leading scientists and journals have already highlighted this study. For example, in the news section of Science magazine, Jon Cohen underlined the originality of the approach for virus hunting on Earth with the title “Armed with air samplers, rope tricks, and—yes—ants, virus hunters spot threats in new ways”[4]. Another example is the mention of the publication by Elisabeth Bik in her Microbiome Digest: she wrote, “An amazing read is a fresh preprint from Fritz and collaborator describing an exciting method of sampling in difficult-to-reach environments“ [5].

The paper from Fritz et al [2] thus represents a significant advance in virus ecology, as already recognized by early readers, and this is why I strongly recommend its publication in PCI Infections.

REFERENCES

1. Edgar RC, Taylor J, Lin V, Altman T, Barbera P, Meleshko D, Lohr D, Novakovsky G, Buchfink B, Al-Shayeb B, Banfield JF, de la Peña M, Korobeynikov A, Chikhi R, Babaian A (2022) Petabase-scale sequence alignment catalyses viral discovery. Nature, 602, 142–147. https://doi.org/10.1038/s41586-021-04332-2

2. Fritz M, Reggiardo B, Filloux D, Claude L, Fernandez E, Mahé F, Kraberger S, Custer JM, Becquart P, Mebaley TN, Kombila LB, Lenguiya LH, Boundenga L, Mombo IM, Maganga GD, Niama FR, Koumba J-S, Ogliastro M, Yvon M, Martin DP, Blanc S, Varsani A, Leroy E, Roumagnac P (2023) African army ants at the forefront of virome surveillance in a remote tropical forest. bioRxiv, 2022.12.13.520061, ver. 4 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.12.13.520061

3. François S, Filloux D, Fernandez E, Ogliastro M, Roumagnac P (2018) Viral Metagenomics Approaches for High-Resolution Screening of Multiplexed Arthropod and Plant Viral Communities. In: Viral Metagenomics: Methods and Protocols Methods in Molecular Biology. (eds Pantaleo V, Chiumenti M), pp. 77–95. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-7683-6_7

4. Cohen J (2023) Virus hunters test new surveillance tools. Science, 379, 16–17. https://doi.org/10.1126/science.adg5292

5. Ponsero A (2023) February 18th, 2023. Microbiome Digest - Bik’s Picks. https://microbiomedigest.com/2023/02/18/february-18th-2023/

African army ants at the forefront of virome surveillance in a remote tropical forestMatthieu Fritz, Berenice Reggiardo, Denis Filloux, Lisa Claude, Emmanuel Fernandez, Frederic Mahe, Simona Kraberger, Joy M. Custer, Pierre Becquart, Telstar Ndong Mebaley, Linda Bohou Kombila, Leadisaelle H. Lenguiya, Larson Boundenga, Illich M. M...<p style="text-align: justify;">In this study, we used a predator-enabled metagenomics strategy to sample the virome of a remote and difficult-to-access densely forested African tropical region. Specifically, we focused our study on the use of arm...Ecohealth, Ecology of hosts, infectious agents, or vectors, One Health, Reservoirs, VirusesSebastien Massart2022-12-14 11:57:40 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 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
06 Apr 2023
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Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations

Changes in aggressiveness in pathotypes of wheat leaf rust

Recommended by based on reviews by 2 anonymous reviewers

Understanding the ecological and evolutionary factors underlying the spread of new fungal pathogen populations can inform the development of more effective management strategies. In plant pathology, pathogenicity is generally presented as having two components: ‘virulence’ (qualitative pathogenicity) and aggressiveness (quantitative pathogenicity). Changes in virulence in response to the deployment of new resistant varieties are a major driver of the spread of new populations (called pathotypes, or races) in modern agrosystems, and the genomic (i.e. proximal) and eco-evolutionary (i.e. ultimate) factors underlying these changes are well-documented [1,2,3]. By contrast, the role of changes in aggressiveness in the spread of pathotypes remains little known [4].

The study by Cécilia Fontyn and collaborators [5] set out to characterize changes in aggressiveness for isolates of two pathotypes of the wheat leaf rust (Puccinia triticina) that have been dominant in France during the 2005-2016 period. Isolates were genetically characterized using multilocus microsatellite typing and phenotypically characterized for three components of aggressiveness on wheat varieties: infection efficiency, latency period, and sporulation capacity. Using experiments that represent quite a remarkable amount of work and effort, Fontyn et al. showed that each dominant pathotype consisted of several genotypes, including common genotypes whose frequency changed over time. For each pathotype, the genotypes that were more common initially were replaced by a more aggressive genotype. Together, these results show that changes in the genetic composition of populations of fungal plant pathogens can be associated with, and may be caused by, changes in the quantitative components of pathogenicity. This study also illustrates how extensive, decade-long monitoring of fungal pathogen populations, such as the one conducted for wheat leaf rust in France, represents a very valuable resource for research.

REFERENCES

[1] Brown, J. K. (1994). Chance and selection in the evolution of barley mildew. Trends in Microbiology, 2(12), 470-475. https://doi.org/10.1016/0966-842x(94)90650-5

[2] Daverdin, G., Rouxel, T., Gout, L., Aubertot, J. N., Fudal, I., Meyer, M., Parlange, F., Carpezat, J., & Balesdent, M. H. (2012). Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathogens, 8(11), e1003020. https://doi.org/10.1371/journal.ppat.1003020

[3] Gladieux, P., Feurtey, A., Hood, M. E., Snirc, A., Clavel, J., Dutech, C., Roy, M., & Giraud, T. (2015). The population biology of fungal invasions.Molecular Ecology, 24(9), 1969-86. https://doi.org/10.1111/mec.13028

[4] Fontyn, C., Zippert, A. C., Delestre, G., Marcel, T. C., Suffert, F., & Goyeau, H. (2022). Is virulence phenotype evolution driven exclusively by Lr gene deployment in French Puccinia triticina populations?. Plant Pathology, 71(7), 1511-1524. https://doi.org/10.1111/ppa.13599

[5] Fontyn, C., Meyer, K. J., Boixel, A. L., Delestre, G., Piaget, E., Picard, C., Suffer, F., Marcel, T.C., & Goyeau, H. (2022). Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations. bioRxiv, 2022.08.29.505401, ver. 3 peer-reviewed and recommended by Peer Community in Infections.  https://doi.org/10.1101/2022.08.29.505401

Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populationsCécilia FONTYN, Kevin JG MEYER, Anne-Lise BOIXEL, Ghislain DELESTRE, Emma PIAGET, Corentin PICARD, Frédéric SUFFERT, Thierry C MARCEL, Henriette GOYEAU<p style="text-align: justify;">Plant pathogens are constantly evolving and adapting to their environment, including their host. Virulence alleles emerge, and then increase, and sometimes decrease in frequency within pathogen populations in respon...Coevolution, Epidemiology, Evolution of hosts, infectious agents, or vectors, Interactions between hosts and infectious agents/vectors, Pathogenic/Symbiotic Fungi, Phytopathology, Plant diseases, Population dynamics of hosts, infectious agents, or...Pierre Gladieux, Jacqui Shykoff, , 2022-09-29 20:01:57 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
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
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 ORCID_LOGO 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