Signatures of gene transfer in the parallel evolution of osmotrophic specialization in eukaryotes

nature ecology & evolution Article https://doi.org/10.1038/s41559-026-03054-w Signatures of gene transfer in the parallel evolution of osmotrophic specialization in eukaryotes Received: 29 May 2025 Accepted: 19 March 2026 Published online: xx xx xxxx Check for updates Eduard Ocaña-Pallarès 1,2,3,4,5 , Thomas A. Richards Toni Gabaldón 3,4,7,8,11 & Gergely J. Szöllősi 9,10,11 , 6 Recurrent transitions in feeding strategies have shaped the eukaryotic tree of life, as unrelated groups independently evolved similar solutions to common ecological challenges. One of the most interesting yet poorly studied of these shifts is the transition towards osmotrophy. We reconstructed the evolution of four eukaryotic groups that specialized in osmotrophy through convergent evolution. Here we show that these groups arose most likely during the Tonian period (1,000–720 million years ago) or slightly before, and possess a genetic toolkit enriched in shared metabolic functions. We report signatures that are compatible with horizontal gene transfer encompassing at least 20% of this toolkit. Phylogenetic reconciliation analyses show that this fraction of the toolkit ranks in the upper percentiles for inferred horizontal gene transfers, particularly in the period in which the osmotrophic groups originated. Moreover, analyses of the total gene content using supervised phylogenetic screening identified 166 gene tree topologies that are supportive of transfer events involving distantly related eukaryotic osmotrophs. These data include transfer highways between Fungi and Pseudofungi and between Labyrinthulea and Teretosporea. Our work thus unravels the evolutionary history of four independent transitions towards specialization in osmotrophy within the eukaryotes, supporting a role of gene transfer in the evolution of these groups. The evolutionary history of eukaryotes is punctuated by major trophic transitions, where shared ecologies have driven distant lineages to evolve analogous forms and functions1,2. One of the most interesting yet poorly studied of these shifts is the transition from a phagotrophic ancestral state of engulfing prey3–6 to specialized osmotrophy7,8. Osmotrophy is a form of heterotrophic nutrition based on the absorption of nutrients directly from the environment, often via extracellular digestion of complex molecules, without relying on phagocytosis7. While this strategy is to some extent present in many organisms, some groups have independently evolved a series of adaptations that allow them to specialize in this trophic mode7,9. Among eukaryotes, Fungi10 are a classic example of forms that specialize in osmotrophy, yet other groups such as Teretosporea11–13, Pseudofungi14,15 and Labyrinthulea16,17 are morphologically similar to Fungi because they also specialize in osmotrophy. On the one hand, Fungi and the Teretosporea clade (Ichthyosporea and Corallochytrea) UOC-TECH, Universitat Oberta de Catalunya, Barcelona, Spain. 2Department of Biological Physics, Eötvös Loránd University, Budapest, Hungary. BSC-CNS, Barcelona Supercomputing Center, Barcelona, Spain. 4Institute for Research in Biomedicine, The Barcelona Institute of Science and Technology, Barcelona, Spain. 5Departament de Medicina i Ciències de la Vida, Institut de Biologia Evolutiva (CSIC-UPF), Universitat Pompeu Fabra, Barcelona, Spain. 6Department of Biology, University of Oxford, Oxford, UK. 7Catalan Institution for Research and Advanced Studies, Barcelona, Spain. 8 Centro de Investigación Biomédica En Red de Enfermedades Infecciosas, Barcelona, Spain. 9Model-Based Evolutionary Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan. 10HUN-REN Centre for Ecological Research, Institute of Evolution, Budapest, Hungary. 11These authors contributed equally: Toni Gabaldón, Gergely J. Szöllősi. e-mail: 1 3 Nature Ecology & Evolution Article https://doi.org/10.1038/s41559-026-03054-w Group age ≥t (% of chronograms) 1 1 Multicellular algae fossil (eukaryotes) 2 Origin of osmotrophic groups 100 2 3 4 3 Metazoa fossil 75 4 Embryophyta fossil Osmotrophic groups 50 Teretosporea 25 Total group Fungi Labyrinthulea Crown group Pseudofungi 0 2,500 2,000 1,500 1,000 500 0 Time (t) in Ma Fig. 1 | Timing the origin of Teretosporea, Fungi, Labyrinthulea and Pseudofungi, four eukaryotic groups that experienced parallel transitions towards osmotrophic specialization. The curves represent the proportion of post-burn-in sampled chronograms from relaxed molecular clock analyses (n = 32,379) in which the estimated age of a group is greater than or equal to the time indicated on the x axis. The dashed black lines show the ages of old bona fide fossils of multicellular eukaryotic algae (Bangiomorpha pubescens, ~1,030 Ma), animals (Charnia masoni, ~575 Ma) and vascular plants (Cooksonia barrandei, ~430 Ma), as described in the key. belong to the Opisthokonta group from the Amorphea division of eukaryotes13. Members of Teretosporea are frequently found as parasites or symbionts of various animals12,18, although free-living representatives have been described11,12,19. Although some Teretosporea were historically misclassified11,20,21 owing to fungal-like morphology, they are phylogenetically closer to animals than to Fungi13. On the other hand, Labyrinthulea16,17 and Pseudofungi14,15 belong to the Stramenopiles22 group from the Diaphoretickes division of eukaryotes6. Labyrinthulea includes saprotrophic species as well as symbionts of algae, marine plants and animals16. Similar to ichthyosporeans19, some species have been described as parasites, commensals or mutualists of invertebrates16. Regarding Pseudofungi (Hyphochytriomycota and Oomycota)14,15,23, Hyphochytriomycota are widespread in occurrence, and most are saprotrophs or parasites15. Oomycetes are numerous in marine, freshwater and terrestrial ecosystems, where they occur as widespread saprotrophs or parasites, and the early diverging groups are almost exclusively marine15. We refer to these four groups (Fungi, Teretosporea, Pseudofungi and Labyrinthulea), which represent a broad diversity of osmotrophic forms, hereafter as ‘osmotrophic groups’. Historically, the shared phenotypic traits among the four osmotrophic groups have led to frequent taxonomic misidentifications and the misclassification of various species (for example, refs. 11,20,21,24,25). These phenotypic similarities include a range of functionally connected traits that allowed species from these groups to specialize into an osmotrophic lifestyle: (1) robust cell wall structures encapsulating the cell and enabling maintenance of high intracellular turgor7, (2) heterotrophy via specialized absorptive nutrition, with adapted secretomes for external digestion of large compound chains7,26–28, (3) hyphae and hyphae-like structures, which often coevolve with specialized osmotrophic lifestyles. They are particularly common in Fungi29 and in some Pseu (...truncated)