From seagrass roots to saline soils: discovery of two new genera in Lulworthiales (Sordariomycetes) from osmotically stressed habitats

As part of an ongoing study of marine fungi associated with seagrasses, we discovered a novel root-fungus symbiosis in the Indo-Pacific species <i>Thalassodendronciliatum</i> 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 <i>Lulworthiales</i>, which are introduced here as <i>Thalassodendromycespurpureus</i> <b>gen. et sp. nov.</b> and <i>Halomyrmapluriseptata</i> <b>gen. et sp. nov.</b>, respectively. Both species developed characteristic structures under culture conditions that enabled their morphological characterisation: <i>T.purpureus</i> forms distinctive clusters of dark brown monilioid hyphae, while <i>H.pluriseptata</i> is characterised by holoblastic conidiogenesis and solitary, dark brown, multicellular conidia. <i>Thalassodendromyces</i> clustered in a strongly supported clade with <i>Spathulospora</i>, a parasitic genus of the red macroalga <i>Ballia</i>, while the closest relatives of <i>Halomyrma</i> were identified as the asexual genera <i>Halazoon</i> and <i>Halophilomyces</i> (nom. inval. Art. 40.7). An analysis of published metabarcoding ITS rDNA data from environmental samples in the GlobalFungi database indicated that <i>H.pluriseptata</i> 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 <i>T.purpureus</i> 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 <i>Lulworthiales</i>, bridging marine and terrestrial fungal communities, and highlight seagrass roots as an important source of novel symbiotic marine fungi. Recent discoveries of the <i>Lulworthiales</i> 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 <i>Spathulosporales</i> 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.