A groundbreaking study using ants revealed a spectacular diversity of viruses in hardly accessible ecosystems like tropical forests
African army ants at the forefront of virome surveillance in a remote tropical forest
Recommendation: posted 23 February 2023, validated 27 February 2023
Massart, S. (2023) A groundbreaking study using ants revealed a spectacular diversity of viruses in hardly accessible ecosystems like tropical forests. Peer Community In Infections, 100077. https://doi.org/10.24072/pci.infections.100077
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 .
In their exciting study, Fritz and collaborators , 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 , 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”. 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“ .
The paper from Fritz et al  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.
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/
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
The study was funded by the Word Organization for Animal Health (EBO-SURSY: FOOD/2016/379-660)
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.12.13.520061
Version of the preprint: 1
Author's Reply, 16 Feb 2023
Decision by Sebastien Massart, posted 07 Feb 2023, validated 07 Feb 2023
On behalf of the board of Peer Community in Infection, I would like to thank you for considering it for sending your publication.
I am please to send you the decision related to the publication sent to Peer Community In Infection whose title is "African army ants at the forefront of virome surveillance in a remote tropical forest". The publication is accepted in PCI Infection and we propose several improvements in the next sections.
The document has been reviewed positively by both reviewers and I have also added some suggestions after reading carefully the manuscript. We have all appreciated the originality of the work and the clarity of the document which is well written taking into account the huge amount of results and discoveries from this innovative approach.
You can find the comments and suggestions of both reviewers and myself in this response and we thank you in advance for answering these point by point while adapting the text when necessary.
Comments from the recommender:
- 87 millions of eukaryotic virus species on earth
This number is an estimation of the number of viral species per eukaryotic species multiplied by the estimation of eukaryotic species on earth. This double estimation has a very large uncertainty and I suggest to eliminate the number but simply indicating there are millions of viruses which already illustrates the gaps with ICTV recognized species
- The organisms that we farm
Thamed organisms, being animals or plants could better represent the borders as dogs or cats are not farmed for example
2. Material and methods
- Positive and negative controls have been used, which is very positive and can rise the confidence in the obtained results but what were the positive and negative controls used ?
- The minimal length of the contig is well justified but the e-value threshold not. Can it be explained ? Indeed, there might be a risk of detecting Enogenous Viral Elements (EVEs) from genome sequences of the hosts with such value.
- How can the link be done between the supplementary table 1 (identifying each sample) and the raw data presented in SRA, more specifically the internal tags identifying each sample within a library (e.g. the 3 pooled sequencing dataset MGN-1, MGN-2 and MGN-3 by Illumina and Flongle sequencing)) ? I could not find it. So adding a column in Supplementary table 1 with the corresponding tags used would facilitate reanalysis of the data of this pioneering sequencing effort by the scientific community
- There is no information on the results of the controls and how it helped in results interpretation (as it has been considered as the third step of bioinformatic analysis in a recent publication – DOI: 10.24072/pcjournal.181 - and in a new EPPO standard PM7/151.
- This point is related to reviewer 1 comment concerning the ~24,000 contigs potentially of viral origin but without similarity to viral genera recognized by ICTV: what to do with them ? They are not really discussed while they could have a great interest in filling the knowledge gaps between existing viruses on earth and already discovered ones (although I acknowledge it is important to remain cautious about them and not being too speculative).
- Were PeVD and SoMV the only known plant viruses detected ?
- While using VANA, how do you explain the small contigs retrieved from plant viruses ? It means complete viral particles were not recovered or the sequencing depth was not high enough as the initial concentrations of the plant viruses were too low ? This could be discussed (maybe more broadly for viruses infecting non-arthropod hosts)