Bacteria Associated With Shiraia Fruiting Bodies Influence Fungal Production of Hypocrellin A

Abstract

Hypocrellin A (HA) is a natural red perylenequinone pigment from Shiraia fruiting body, which was used clinically on various skin diseases and developed as a photodynamic therapy agent against cancers. The fruiting bodies may harbor a diverse but poorly understood microbial community. In this study, we characterized the bacterial community of Shiraia fruiting body using a combination of culture-based method and Illumina high-throughput sequencing, and tested the involvement of some companion bacteria in fungal HA production using the fungal–bacterial confrontation assay. Our results revealed that the bacterial community in the fruiting body was dominated by Bacillus and Pseudomonas. Some Pseudomonas isolates such as P. fulva, P. putida, and P. parafulva could stimulate fungal HA accumulation by Shiraia sp. S9. The bacterial treatment of P. fulva SB1 up-regulated the expression of polyketide synthase (PKS) for HA biosynthesis and transporter genes including ATP-binding cassette (ABC) and major facilitator superfamily transporter (MFS) for HA exudation. After the addition of live P. fulva SB1, the mycelium cultures of Shiraia sp. S9 presented a higher HA production (225.34 mg/L), about 3.25-fold over the mono-culture. On the other hand, B. cereus was capable of alleviating fungal self-toxicity from HA via down-regulation of HA biosynthetic genes or possible biodegradation on HA. To our knowledge, this is the first report on the diversified species of bacteria associated with Shiraia fruiting bodies and the regulation roles of the companion bacteria on fungal HA biosynthesis. Furthermore, the bacterial co-culture provided a good strategy for the enhanced HA production by Shiraia.

Nitric Oxide and Hydrogen Peroxide Signaling in Extractive Shiraia Fermentation by Triton X-100 for Hypocrellin A Production

“…The intracellular HA was secreted into its fermentation broth ( Figure 1E) and consecutively extracted into the nonaqueous micelle phase ( Figure 1A). Since HA was confirmed to be self-toxic to the fungus in our recent paper [27], the transferring of HA into its nonionic surfactant micelle aqueous solution in extractive fermentation may alleviate self-toxicity of HA on fungal growth or the feedback inhibition of HA biosynthesis. Our results also demonstrated that increase of HA production in the extractive fermentation was from not only HA in the cultural broth, but also the stimulated biosynthesis of HA in mycelial cells (Figure 1).…”

Phylogenetic Position of Shiraia-Like Endophytes on Bamboos and the Diverse Biosynthesis of Hypocrellin and Hypocrellin Derivatives

“…Those from fruit bodies of S. bambusicola BJTC HOU999 and R. bambusae BJTC HOU1000 only produced hypocrellins, and that from R. bambusae BJTC HOU1000 (65.89 mg/g) produced a higher quantity of hypocrellins than S. bambusicola BJTC HOU999 (10.39 mg/g). It is noteworthy that the extracts from P. conidialis CNUCC 1353PR contained a large concentration of natural products, and both the total perylenequinonoid compound content (1410.13 mg/L) and that of the single compound HA (677.11 mg/L) showed a substantially higher quantity than any other known wild type strains in public papers [ 49 , 50 , 51 , 52 ].…”

Nitric oxide donor sodium nitroprusside-induced transcriptional changes and hypocrellin biosynthesis of Shiraia sp. S9

“…The strain Shiraia sp. S9 (CGMCC16369) for hypocrellin production was obtained from fresh Shiraia fruit-body in our previous work [ 49 ]. The strain was maintained and stored at 4 °C on a potato dextrose agar (PDA) slant and initially grown at 28 °C for 8 days.…”