Lipopolysaccharides from a Shiraia fruiting body-associated bacterium elicit host fungal hypocrellin A biosynthesis through nitric oxide generation

Hypocrellin A (HA) is an excellent perylenequinone photosensitizer from Shiraia fruiting bodies. A dominant bacterium Pseudomonas fulva SB1 in the fruiting body was found to promote HA biosynthesis. The bacterial LPS were purified and the O-specific polysaccharide (OPS) consisted of rhamnose (Rha), galactose (Gal) and N-acetyl-galactosamine (GalNAc) with an average molecular weight of 282.8 kDa. Although the OPS composing of Rhap and Galp backbone showed elicitation capability on fungal HA accumulation, the highest HA production (303.76 mg/L) was achieved by LPS treatment at 20 mu g/mL on day 3 of the mycelium culture. The generation of nitric oxide (NO) in Shiraia mycelia was triggered by LPS, which was partially blocked by inhibitors of nitric oxide synthase (NOS) and nitrate reductase (NR), leading to the depressed HA production. Transcriptome analysis revealed that NO mediated LPS-induced HA production via upregulating the expressions of critical genes associated with central carbon metabolism and downstream HA biosynthesis genes. This is the first report of LPS-induced NO to regulate fungal secondary metabolite production, which provides new insights on the role of bacterial LPS in bacterium-fungus interactions and an effective strategy to enhance hypocrellin production.