Palmitoleic acid as a coordinating molecule between the invasive pinewood nematode and its newly associated fungi

Abstract

Abstract Symbiotic microorganisms are ubiquitous on the body surface or internal tissues of invertebrates, providing them with benefits. Developing symbiotic relationships requires synchronization of developmental stages and physical proximity of partners. Therefore, the identification of metabolites that coordinate the reproduction of symbiotic partners is essential. This study demonstrates that palmitoleic acid (C16: 1) coordinates bilateral propagation by regulating the synchronization of reproduction between the invasive pinewood nematode (PWN) and its newly associated blue-stain fungus, Sporothrix sp.1. When the PWN fed on Sporothrix sp.1, there was a significant increase in lipid metabolism gene expression and metabolite abundance. Through further investigations, it highlighted a significant enhancement in the reproduction of the PWN through direct acquisition of C16: 1, which was abundantly present in Sporothrix sp.1. Furthermore, the PWN biosynthesized C16: 1 through the involvement of the stearoyl-CoA 9-desaturase gene fat-5 and its hormone nuclear receptor nhr-80, which was clarified to promote the egg-laying capacity of females. Moreover, it is worth noting that the production of C16: 1 was significantly higher by the associated fungus Sporothrix sp.1 to enhance sporulation during the spore formation phase compared to the hypha growth phase. Thus, by coordinating the fecundity and spore production, the key lipid metabolite C16: 1 facilitates the rapid and successful colonization of a mutually beneficial symbiotic relationship between the invasive PWN and the native Sporothrix sp.1 within the host. This finding emphasizes the significant role of metabolite sharing and its function in promoting partner synchronization within symbiotic relationships.