As part of an ongoing study of marine fungi associated with seagrasses, we discovered a novel root-fungus symbiosis in the Indo-Pacific species Thalassodendronciliatum from Mauritius. Culturing its mycobionts yielded dozens of morphologically and genetically uniform isolates, all representing a previously unknown fungus. A second undescribed fungus was isolated from saline soils in Czechia. Phylogenetic analyses based on three rDNA markers confirmed both taxa as distinct, hitherto unknown lineages within the Lulworthiales, which are introduced here as Thalassodendromycespurpureus gen. et sp. nov. and Halomyrmapluriseptata gen. et sp. nov., respectively. Both species developed characteristic structures under culture conditions that enabled their morphological characterisation: T.purpureus forms distinctive clusters of dark brown monilioid hyphae, while H.pluriseptata is characterised by holoblastic conidiogenesis and solitary, dark brown, multicellular conidia. Thalassodendromyces clustered in a strongly supported clade with Spathulospora, a parasitic genus of the red macroalga Ballia, while the closest relatives of Halomyrma were identified as the asexual genera Halazoon and Halophilomyces (nom. inval. Art. 40.7). An analysis of published metabarcoding ITS rDNA data from environmental samples in the GlobalFungi database indicated that H.pluriseptata is widely distributed across temperate, subtropical, and tropical regions in the Northern and Southern Hemispheres. The species exhibits a strong preference for aquatic biomes, particularly marine and estuarine, with a few records in terrestrial ecosystems. In contrast, no record of T.purpureus was retrieved from GlobalFungi, suggesting narrower ecological specialisation, a close association with its seagrass host, and/or a restricted geographical range. Our findings expand the ecological and phylogenetic scope of the Lulworthiales, bridging marine and terrestrial fungal communities, and highlight seagrass roots as an important source of novel symbiotic marine fungi. Recent discoveries of the Lulworthiales in saline inland soils challenge their marine exclusivity and raise important questions about their ecological plasticity, dispersal mechanisms, and adaptive strategies. In light of current observations, we discuss the taxonomic challenges of the Spathulosporales and the lulworthialean fungi, integrating molecular and morphological perspectives. We address the importance of combining morphological and molecular approaches to accurately delineate new fungal taxa, as well as the value of environmental DNA metabarcoding for uncovering cryptic fungal diversity and enhancing our understanding of fungal distribution and ecological functions.

• Keywords
• Dictyoconidia, Thalassodendron, holoblastic conidiogenesis, marine, monilioid, new taxa, phylogenetics, saprobic, symbiotic,
• Publication type
• Journal Article MeSH

Symbioses with fungi are important and ubiquitous on dry land but underexplored in the sea. As yet only one seagrass has been shown to form a specific root-fungus symbiosis that resembles those occurring in terrestrial plants, namely the dominant long-lived Mediterranean species Posidonia oceanica (Alismatales: Posidoniaceae) forming a dark septate (DS) endophytic association with the ascomycete Posidoniomyces atricolor (Pleosporales: Aigialaceae). Using stereomicroscopy, light and scanning electron microscopy, and DNA cloning, here we describe a novel root-fungus symbiosis in the Indo-Pacific seagrass Thalassodendron ciliatum (Alismatales: Cymodoceaceae) from a site in the Gulf of Aqaba in the Red Sea. Similarly to P. oceanica, the mycobiont of T. ciliatum occurs more frequently in thinner roots that engage in nutrient uptake from the seabed and forms extensive hyphal mantles composed of DS hyphae on the root surface. Contrary to P. oceanica, the mycobiont occurs on the roots with root hairs and does not colonize its host intraradically. While the cloning revealed a relatively rich spectrum of fungi, they were mostly parasites or saprobes of uncertain origin and the identity of the mycobiont thus remains unknown. Symbioses of seagrasses with fungi are probably more frequent than previously thought, but their functioning and significance are unknown. Melanin present in DS hyphae slows down their decomposition and so is true for the colonized roots. DS fungi may in this way conserve organic detritus in the seagrasses' rhizosphere, thus contributing to blue carbon sequestration in seagrass meadows.

• Keywords
• Blue carbon sequestration, Dark septate endophytes, Epiphytism, Marine fungi, Necromass decomposition, Nutrient uptake, Root-fungus symbioses, Seagrasses,
• MeSH
• Alismatales * microbiology   physiology   MeSH
• Ascomycota physiology   MeSH
• Plant Roots * microbiology   MeSH
• Symbiosis * MeSH
• Publication type
• Journal Article MeSH
• Geographicals
• Indian Ocean MeSH