Mots-Clés
funhal genomics
mobile elements
fermented food
starship
Description
The role of Starships in iron uptake
Supervisors, addresses, e-mails, URLs:
Jeanne Ropars ; Laboratoire Ecologie Société Evolution UMR8079 Université Paris-Saclay, CNRS, AgroParisTech, 12 route 128, 91190 Gif-sur-Yvette ; jeanne.ropars@cnrs.fr ;
Vincent Hervé ; Université Paris-Saclay, INRAE, AgroParisTech, UMR SayFood, 91120 Palaiseau, France ; vincent.herve@inrae.fr ; https://orcid.org/0000-0002-3495-561X
Address of the internship location: UMR SayFood, équipe CoMiAl. 22 place de l’agronomie, 91120 Palaiseau, France
Possibility of a PhD proposal on/related to the internship subject: Yes
Publications of the supervisors related to the proposal:
- Mekuli, R., Shoukat, M., Dugat-Bony, E., Bonnarme, P., Landaud, S., Swennen, D., & Hervé, V. (2025). Iron-based microbial interactions: the role of iron metabolism in the cheese ecosystem. Journal of Bacteriology, 207(5), e00539-24.
- Shoukat, M., Hervé, V., Sarthou, A. S., Peron, A. C., Danel, A., Swennen, D., … & Dugat-Bony, E. (2025). Iron fortification modifies the microbial community structure and metabolome of a model surface-ripened cheese. International Journal of Food Microbiology, 427, 110971.
- O’Donnell, S., Rezende, G., Vernadet, J.-P., Snirc, A., & Ropars J. (2025). Harboring Starships : the accumulation of large horizontal gene transfers in domesticated and pathogenic fungi. Genome Biology and Evolution, 17(7), evaf125.
DESCRIPTION
INTRODUCTION, SCIENTIFIC CONTEXT:
Understanding how organisms adapt to their environment is a central question in evolutionary biology. Because environments include many organisms, biotic interactions are a key component of ecological niches, encompassing beneficial, neutral and antagonistic interactions. Microorganisms, in particular, form complex communities shaped by their interactions, which in turn drive adaptation. Among microorganisms, fungi are excellent eukaryotic models for studying interaction and adaptation, as they combine strong experimental assets (e.g. small genomes and ease to manipulate in laboratory conditions), with a remarkable diversity, ranging from unicellular yeasts to multicellular molds. Yet, they have rarely been used to investigate biological interactions, and the mechanisms underlying fungal interactions and rapid adaptation remain poorly understood.
Horizontal gene transfer (HGT), i.e. the non-sexual transfer of genetic material between genomes, has long been recognized as a major driver of prokaryotic evolution and adaptation, and more recently as a significant contributor to eukaryotic microbial genomes. New acquired elements can confer strong fitness benefits to the host genome, such as competitive advantages over other organisms. A newly described superfamily of giant transposable elements, named Starships, has been detected across many fungal lineages (Urquhart et al., 2024). Starships are detected by presence/absence polymorphisms between strains/species. These elements appear to play key roles in rapid adaptation, by shuttling cargo genes not only between strains but even across species. Strikingly, many transferred genes are involved in biotic interactions, including virulence effector genes whose horizontal transfer has enabled fungi to produce host-targeting toxins and colonize plants (e.g. (Bucknell et al., 2025)). One of the teams involved in this project has also previously shown that adaptation of Penicillium fungi to cheese, dry-cured meat and other food occurred through horizontal gene transfers, mediated by Starships, and in particular for traits related to competition: some Starship cargo genes in Penicillium cheese and dry-cured meat fungi allow more efficient use of nutrients, thus providing an advantage in the competition against other microorganisms(O’Donnell et al., 2025). Starships are particularly abundant in domesticated lineages compared to their wild counterparts, supporting their role in rapid adaptation to new environments (O’Donnell et al., 2025). Notably, previous findings have revealed that more than 15% of the genome of the emblematic cheese species P. camemberti, used for making soft cheeses, is made up of Starship material when compared to its wild counterpart (O’Donnell et al., 2025). Cargo genes in P. camemberti were enriched in functions relevant for adaptation, in particular in relationship to nutrient uptake, including iron which is sparse in cheese. Other fungal genera are recurrently found in cheese, such as Scopulariopsis. Preliminary analyses on Scopulariopsis led by the hosting lab revealed multiple Starships shared between strains and even across species, while absent from closely related non-cheese strains. More comprehensive analyses across these fungi are now needed, in particular to investigate the role of Starships in adaptation and biotic interactions.
Fermented products provide valuable systems for studying microbial interactions, as they form relatively simple ecosystems, where various microbial groups co-occur or succeed one another. Artisanal cheeses are particularly powerful models: their rind communities, unlike industrial products, arise naturally without inoculation, preventing domination by a single strain and fostering diverse, balanced interactions. Artisanal cheeses possess a diverse microbiota composed of bacteria, fungi and viruses that engage into various types of interactions during the cheese-making process. While cheese can be seen as a rich substrate in terms of lipids and proteins, some essential micronutrient can be limiting for microbial growth. This is the case of iron, which is sparse (median concentration of 2.9 mg/kg) and with limited bioavailability due to the presence of various metal-binding agents in the cheese matrix (Mekuli et al., 2025). As such, iron is key for various microbial interactions in cheese. Thus, microorganisms able to produce and/or import ferric iron-specific chelators called siderophores possess a competitive advantage. Additionally, horizontal transfer of siderophore acquisition genes has been reported in cheese bacteria (Bonham et al., 2017). However, in the case of cheese fungi, the diversity, origin and dynamics of siderophore biosynthesis and import have been overlooked.
RESEARCH PROPOSAL/OBJECTIVES:
The present project aims at investigating adaptation, by exploring the role of Starships in biotic interactions across phylogenetically distant cheese fungi. Key questions are: do horizontal gene transfers underlie rapid adaptation and interactions in cheese? What functions do Starship cargo genes encode? In particular, are siderophores located in Starships?
The student will i) analyze Starships and other HGTs in Scopulariopsis genomes; (ii) identify iron acquisition systems, especially within Starships, using curated HMMs; (iii) assess the diversity of iron-related HGTs; (iv) infer the origins of Starships and iron uptake genes; (v) validate gene functions experimentally.
DESCRIPTION OF DATA if applicable (Data must be available before the start of the internship):
The hosting labs have a large collection of more than 150 unpublished Scopulariopsis genomes (long reads and short reads) of strains/species isolated from cheese and other environments. Other cheese-associated fungal genomes are also available from the hosting labs and could be used too. Fungal genomes from closely related species and from other environments will be extracted from public databases such as NCBI and MycoCosm. We will also use the STARBASE database and toolkit (https://starbase.serve.scilifelab.se/), which catalogs all Starships found in fungal species worldwide.
METHODOLOGIES:
This project will mostly involve in silico analyses including data mining, comparative genomics, phylogenetic and statistical analyses. Depending on the results of these analyses, fungal strains will be tested in the lab. Wet lab experiment will include growth measurement at various iron concentrations, phenotypic tests for the production of siderophores and the chemical characterization of these siderophore using the MetaVolFood plateform.
REFERENCES
Bonham, K.S., Wolfe, B.E., Dutton, R.J., 2017. Extensive horizontal gene transfer in cheese-associated bacteria. eLife 6, e22144. https://doi.org/10.7554/eLife.22144
Bucknell, A., Wilson, H.M., Gonçalves dos Santos, K.C., Simpfendorfer, S., Milgate, A., Germain, H., Solomon, P.S., Bentham, A., McDonald, M.C., 2025. Sanctuary: a Starship transposon facilitating the movement of the virulence factor ToxA in fungal wheat pathogens. mBio 0, e01371-25. https://doi.org/10.1128/mbio.01371-25
Mekuli, R., Shoukat, M., Dugat-Bony, E., Bonnarme, P., Landaud, S., Swennen, D., Hervé, V., 2025. Iron-based microbial interactions: the role of iron metabolism in the cheese ecosystem. J. Bacteriol. 207, e00539-24. https://doi.org/10.1128/jb.00539-24
O’Donnell, S., Rezende, G., Vernadet, J.-P., Snirc, A., Ropars, J., 2025. Harbouring Starships: The accumulation of large Horizontal Gene Transfers in Domesticated and Pathogenic Fungi. Genome Biol. Evol. evaf125. https://doi.org/10.1093/gbe/evaf125
Urquhart, A., Vogan, A.A., Gluck-Thaler, E., 2024. Starships: a new frontier for fungal biology. Trends Genet. S0168952524001835. https://doi.org/10.1016/j.tig.2024.08.006