Thèse Rôle des Starships dans l'Adaptation Fongique et dans la Mobilisation des Systèmes d'Assimilation du Fer H/F - 75

Établissement : Université Paris-Saclay GS Biosphera - Biologie, Société, Ecologie & Environnement, Ressources, Agriculture & Alimentation
École doctorale : Sciences du Végétal : du gène à l'écosystème
Laboratoire de recherche : Écologie, Société et Évolution
Direction de la thèse : Jeanne ROPARS ORCID 0000000237409673
Début de la thèse : 2026-10-01
Date limite de candidature : 2026-05-04T23:59:59Avec le développement des aliments fermentés comme le fromage, les humains ont créé de nouvelles niches écologiques pour les micro-organismes, les contraignant à s'adapter. L'un des principaux mécanismes d'adaptation repose sur l'acquisition horizontale de matériel génétique. Chez les champignons, ce phénomène peut se produire via les Starships, une superfamille d'éléments transposables géants récemment découverte.
L'un des défis majeurs pour les micro-organismes colonisant le fromage est de surmonter la faible concentration et la faible biodisponibilité du fer, un nutriment essentiel à leur métabolisme. En utilisant Scopulariopsis comme modèle de genre fongique associé au fromage, ce projet exploitera plus de 150 génomes issus d'environnements fromagers et non fromagers afin i) d'identifier des marqueurs d'adaptation au fromage ; ii) d'identifier et de décrypter le rôle des Starships dans cette adaptation ; et iii) d'explorer la diversité des systèmes d'acquisition du fer et leur association avec les Starships. Les principaux résultats obtenus in silico seront ensuite validés par des tests physiologiques in vitro. Ces travaux approfondiront notre compréhension de l'adaptation fongique à de nouvelles niches. La comparaison avec d'autres modèles fongiques associés au fromage, comme les espèces de Penicillium, permettra d'identifier des patterns communs d'adaptation et de tester si une évolution convergente a eu lieu chez les champignons du fromage.

Starships are transforming our understanding of fungal evolution1, acting as major drivers of rapid adaptation. Starships have been identified in plant pathogens, in which cargo genes likely facilitated host shifts2-4, in human pathogens in which cargo genes likely impact virulence and allow strain heterogeneity in clonal populations 5 and in food-associated fungi, where they mediate adaptation and competition in cheese and in dry-cured meat6-9. Yet, Starships have only been very recently discovered, and their distribution and their role in adaptation remain poorly understood. Cheese fungi provide ideal models: multiple phylogenetically distant lineages independently adapted to cheese, with small genomes, ease of cultivation, and hundreds of strains and genomes available. In the cheese ecosystem, an important abiotic driver of microbial community assembly is iron. Indeed, this nutrient is essential to bacterial and fungal metabolism but its concentration and bioavailability is low in cheese10. Therefore, cheese microorganisms rely on various strategies to acquire iron including the production and/or import of ferric iron-specific chelators called siderophores. Among these microbes, filamentous fungi are able to synthesize and import a wide range of siderophores11. Some of these fungal siderophores can also be imported by bacteria, supporting the idea that siderophores act as public goods in cheese. Overall, adaptation to the cheese ecosystem requires the ability to deal with limited iron concentration and Starships could be key to fungal adaptation.

The PhD project aims at investigating adaptation and convergence, by exploring the role of Starships in adaptation across several species of Scopulariopsis cheese fungi and the diversity and origins of iron-uptake genes in cheese fungi. The study will integrate population genomics, comparative genomics and phenotypic tests, to explore how these fungi have evolved in cheese. Using a dataset of over 150 genomes, the student will examine whether the two most common Scopulariopsis species found in cheese, S. asperula and S. flava, have adapted to this niche. The first objective is to test whether Scopulariopsis cheese-associated species have indeed adapted to cheese. The student will 1) assess whether genetic and phenotypic differentiation has occurred between cheese and non-cheese strains, and 2) identify candidate genes and/or genomic regions involved in adaptation. The second objective will focus on horizontal gene transfers, specifically through the identification of Starships (presence/absence polymorphisms) and their cargo-genes, to elucidate their role in adaptation to cheese. Finally, the project will explore iron acquisition systems in environmental fungi and cheese-associated fungi, with a particular emphasis on those located in Starships. Iron import, export and siderophore biosynthesis pathway will be investigated in silico while the capacity to grow at different iron concentrations and to produce siderophores will be tested in vitro.

Understanding how organisms adapt to their environment is a central question in evolutionary biology, and whether adaptation is contingent or repeatable also has major implications. Parallel adaptation, i.e. independent adaptation of multiple lineages to the same environment, provides a powerful way to address these questions.
Fungi are excellent microbial eukaryotic models for studying adaptation, combining strong experimental assets with a remarkable diversity. Yet, they have rarely been used to investigate adaptation, and the mechanisms underlying rapid adaptation remain poorly understood.
Horizontal gene transfer (HGT), i.e. the non-sexual transfer of genetic material between genomes, has been recognized 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. 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. One of the teams involved in this project has also previously shown that adaptation of Penicillium fungi to food, including cheese, occurred through horizontal gene transfers, mediated by Starships. Cargo genes in the emblematic species P. camemberti were enriched in functions relevant for adaptation, in particular in relationship to nutrient uptake, including iron which is sparse in cheese. 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. HGT of iron acquisition genes has already been reported in cheese-associated bacteria. However, the diversity, origin and dynamics of siderophore biosynthesis and import in cheese fungi have been overlooked. Preliminary analyses on Scopulariopsis, a genus recurrently found in cheese, revealed multiple Starships shared between strains and even across species, while absent from closely related non-cheese strains. Notably, some genes within these Starships coded for functions linked to iron uptake. More comprehensive analyses are needed, in particular to investigate the role of Starships in adaptation.
This PhD project aims to investigate adaptation and convergence, leveraging about 150 genome sequences already available in the host lab. It will test whether Starships drive rapid adaptation to novel environments like cheese, and whether convergent adaptation has occurred through independent recruitment of similar genes or functions. The PhD project will also focus on iron acquisition systems in cheese fungi, especially within Starships. Key questions are: do horizontal gene transfers underlie rapid adaptation and interactions in cheese fungi? What functions do Starship cargo genes encode? What are the iron acquisition systems in cheese fungi and in particular in Scopulariopsis? Have similar genes been acquired in phylogenetically distant cheese fungi?
Obj. 1 - Are cheese-associated Scopulariopsis fungi adapted to cheese?
1.1. Adaptation to cheese and the domestication history of Scopulariopsis cheese-associated species
If adaptation has occurred in Scopulariopsis species, we need to determine whether genetic exchange has ceased between cheese and non-cheese strains, which could have led to genetic differentiation at the genome level. Among the six Scopulariopsis species isolated from cheese, two are most common on cheese: S. asperula and S. flava. The PhD student will use population genomics on S. flava and S. asperula, to 1) determine whether genetic subdivisions exist and 2) assess genetic diversity between and/or within cheese and non-cheese populations. Population genomics analyses will make it possible to look for recombination footprints in genomes and to interpret the domestication history of Scopulariopsis cheese-associated species.
Many phenotypic tests have already been performed by the hosting lab on S. asperula and S. flava. In particular, phenotypes were measured for salt tolerance, radial growth on different media, supplemented by different carbon and metal sources, lipolytic and proteolytic activities. Results will be analysed by the PhD student to test whether there is phenotypic differentiation between cheese and non-cheese strains, with strains isolated from cheese having evolved specific traits beneficial for cheesemaking compared to populations from other environments.
1.2. Genomic processes involved in adaptive divergence
A prerequisite to study the genomic processes involved in adaptive divergence in Scopulariopsis species is 1) genetic and phenotypic differentiation between cheese and non-cheese strains, and 2) diversity within the different Scopulariopsis species (Obj. 1.1). If those conditions are met, the student will be able to identify the genomic processes involved in this adaptive divergence using both population genomics and comparative genomics analyses. The comparative genomics approach will enable us to search for specific genomic regions that are only present in cheese strains, and to investigate if they correspond to Starships (objective 2). In this effort, the PhD student will search for regions transferred horizontally between cheese species that could contain key genes for adaptation to cheese. Comparative genomics and population genomics approaches will also identify genes under positive selection involved in adaptation, as well as genomic regions under selective sweeps (only feasible if footprints of recombination are detected in Obj. 1.1). This will enable the detection of recent selection events and allow the targeting of these regions using specific markers in a larger collection of strains.
Obj. 2 - Investigating the presence and polymorphism of Starships and elucidating their role in adaptation
Using a comparative genomics approach, the PhD student will identify Starship presence/absence polymorphisms across the entire Scopulariopsis dataset, which includes over 150 genomes. Both long-read assemblies and short-read genomes will be used. This approach will enable the precise delimitation of Starships and the accurate characterization of their cargo genes. The PhD student will use tools specifically developed for this purpose, including stargraph (https://github.com/SAMtoBAM/stargraph) and starfish12. The catalog of all cargo genes will enable testing for the enrichment of specific functions relevant for cheese adaptation, e.g. salt tolerance, lactose metabolisms, and particularly iron uptake genes (Obj. 3). Laboratory assays may also be conducted to test whether Starships enhance fitness in strains carrying specific Starships, leveraging their presence/absence polymorphisms. Additionally, the PhD student will use the STARBASE database and toolkit (https://starbase.serve.scilifelab.se/), which catalogs all Starships identified in fungal species worldwide. This PhD project will also contribute to expanding this database.
Obj. 3 - What iron-uptake systems have evolved in cheese-associated fungi?
This last objective will challenge the hypothesis that iron acquisition systems are key to the adaptation to the cheese ecosystem, and that part of these systems were obtained via Starships. To do so, the PhD student will use a set of specific Hidden Markov Models (HMMs) recently developed by the hosting lab (https://github.com/STabuteau/iron\_cheese\_metagenomes)11 to identify the iron acquisition systems in the 150 genomes of Scopulariopsis. First, a comparison will be made between cheese and non-cheese fungal genomes to test for a potential enrichment in cheese fungi. Second, the results of this in silico screening will be compared to results of Obj. 2, to detect the iron related genes present in Starships. The capacity of Scopulariopsis strains to grow at different iron concentrations, to import and to produce siderophores will be validated with in vitro tests. Lastly, to generalize his/her results, the PhD student will test the hypothesis of convergent evolution by performing the same in silico analyses on other cheese fungi, especially on two Penicillium species used in cheesemaking, P. camemberti and P. roqueforti. Convergent evolution will be demonstrated if similar patterns, i.e. enrichment of iron acquisition genes in Starships, same genes, are observed between distinct cheese-associated fungal species.