The genome, transcriptome and metabolome of Aspergillus welwitschiae Ocstreb1 from wild halophytic rice, Oryza coarctata, indicates its distinctiveness.
Aspergillus welwitschiae is a widespread fungus with diverse roles as a plant mutualist, opportunistic human pathogen and industrial enzyme producer. The endophytic strain AwOcstreb1, isolated from halophytic rice (Oryza coarctata), promotes growth in commercial rice under normal and saline conditions. Despite its significance, genomic and metabolic resources for A. welwitschiae remain limited, with no complete genome information available for endophytic strains within the species. Moreover, the close relationship of this species to Aspergillus niger complicates its taxonomic resolution. We performed whole-genome and transcriptomic sequencing of AwOcstreb1 cultured on potato dextrose agar, along with -MS-based volatile metabolite profiling. Comparative analyses included simple sequence repeat (SSR), transposable element (TE; including starships) and carbohydrate-active enzyme (CAZyme) profiling across A. welwitschiae strains. Evolutionary relationships with A. niger were examined using average nucleotide identity (ANI) and orthologous gene clustering, supported by phylogenomic reconstruction. Genes for mycotoxin production and plant growth-promoting traits were also searched in this strain. The AwOcstreb1 genome is 37.7 Mb with 13,242 predicted genes, of which 66.6% were actively expressed under potato dextrose agar growth. The genome harbours 5,126 SSRs, 19,434 TEs and a CAZyme composition similar to other A. welwitschiae strains. Although established marker genes such as CaM and β-tubulin identify AwOcstreb1 as A. welwitschiae, whole-genome ANI and orthologous gene-based analyses place A. welwitschiae strains within the broader A. niger species complex, suggesting that it represents a population-level group rather than a clearly separated species, a view that is still not widely adopted. Synteny analysis showed that the AwOcstreb1 genes are highly collinear with those of A. niger. Genes involved in phosphate and zinc solubilization and siderophore biosynthesis were detected, whereas ochratoxin A biosynthetic genes were absent. Although the presence of fumonisin genes was detected, only a trace amount of the toxin was detected both in culture as well as rice grains. Among 172 strain-specific orthogroups, several encode intrinsically disordered, secreted or membrane-associated proteins that are potentially linked to endophytic lifestyle adaptations. Volatile metabolite profiling identified compounds such as 17-pentatriacontene, eicosane and octanal, each linked to known biological sources and potential functions, such as antifungal, antibacterial and anti-inflammatory activities. Several additional metabolites were also identified, whose biological roles need further investigation. This integrated omics study provides foundational insights into the endophytic potential and genomic distinctiveness of AwOcstreb1. This work opens new avenues for exploring A. welwitschiae for sustainable agriculture and fungal biology.