Impact of the Cultivation Technique on the Production of Secondary Metabolites by Chrysosporium lobatum TM-237-S5, Isolated from the Sponge Acanthella cavernosa

Abstract

The fungi Chrysosporium lobatum TM-237-S5 was isolated from the sponge Acanthella cavernosa, collected from the mesophotic coral ecosystem of the Red Sea. The strain was cultivated on a potato dextrose agar (PDA) medium, coupling solid-state fermentation and solid-state extraction (SSF/SSE) with a neutral macroreticular polymeric adsorbent XAD Amberlite resin (AMBERLITE XAD1600N). The SSF/SSE lead to high chemodiversity and productivity compared to classical submerged cultivation. Ten phenalenone related compounds were isolated and fully characterized by one-dimensional and two-dimensional NMR and HRMS. Among them, four were found to be new compounds corresponding to isoconiolactone, (-)-peniciphenalenin F, (+)-8-hydroxyscleroderodin, and (+)-8-hydroxysclerodin. It is concluded that SSF/SSE is a powerful strategy, opening a new era for the exploitation of microbial secondary metabolites.the massive presence of microorganisms in the mesophyl matrix of the sponges, representing around 50% of their biomass [9][10][11].Fungi in the marine environment, and especially those associated with marine invertebrates, have been extensively investigated and reviewed [12,13]. A 2019 collaborative review highlighted the present state of knowledge and raised a multitude of open questions regarding the diversity and function of fungi in marine ecosystems [13].The symbiont assemblages inside the sponge are well organized in biofilms or dense colonies and are stabilized in the skeleton network over time [14,15]. This certainly impacts their development steps and the expression of biosynthetic clusters of secondary metabolites because it is now well documented that, in fungi, secondary metabolism and life cycle among fungi are co-regulated at the genomic level [16][17][18].This idea drives us to compare the metabolic profile of fungi cultivated on a gar slants and in liquid state. The result is that solid-state cultivation often leads to larger molecular diversity than classical liquid state fermentation LSF [19][20][21]. The major obstacle that stands against agar cultivation is the scale-up. In order to overcome such a challenge, we have developed specific innovative technologies, namely Platotex [22,23] and, more recently, Unifertex [24]. As we systematically coupled the culture of microorganisms with in-situ solid phase extraction (SPE), we also developed a specific SPE procedure for agar cultivation, termed solid-solid extraction (SSE) [25].In the present study, we report the impact of agar-supported cultivation on the production of secondary metabolites by the marine fungi Chrysosporium lobatum TM-237-S5, isolated from the Red Sea sponge Acanthella cavernosa. Chrysosporium lobatum was previously reported in the literature as a mosquito pathogenic fungus [26]. However, a very limited number of secondary metabolites have been reported in the literature for the genus Chrysosporium. Thus, the strain Chrysosporium queenslandicum IFM produced naphthaquinone-type altersolanols A, B, and C, the antifungal queenslandon, a representative...

Prioritization of Microorganisms Isolated from the Indian Ocean Sponge Scopalina hapalia Based on Metabolomic Diversity and Biological Activity for the Discovery of Natural Products

“…The results obtained indicated the presence of many compounds directly coming from the culture medium in the microbial extracts. Further experiments should focus on reducing this presence or enriching the extracts in metabolites of interest, using amberlite for instance [ 69 ]. However, this quantitative analysis helps to guide the future isolation, purification and identification work.…”

The Culturable Mycobiome of Mesophotic Agelas oroides: Constituents and Changes Following Sponge Transplantation to Shallow Water

“…Fungi have been repeatedly cultured from a wide variety of sessile marine animals [18]. There has been at least one report of the isolation of a sponge-associated fungus, from Acanthella cavernosa, collected from a mesophotic depth [37]. In the case of Agelas sp., fungi have been, so far, isolated or identified by DDGE analysis from specimens obtained from shallow depths [33,38,39].…”

Discovery of Cymopolyphenols A–F From a Marine Mesophotic Zone Aaptos Sponge-Associated Fungus Cymostachys sp. NBUF082

“…While many researchers have studied macroscopic marine organisms, some natural products they discovered have been suspected or shown to be produced by associated microorganisms ( Hirata and Uemura, 1986 ; Still et al, 2014 ; McCauley et al, 2020 ; Newman and Cragg, 2020 ). Recently, the multinational EU-funded program, TASCMAR (Tools And Strategies to access original bioactive compounds by Cultivating MARine invertebrates and associated symbionts 2 ), has begun to harness of the microbial diversity of some mesophotic zone invertebrates for the purpose of natural products discovery projects, and these have reported new bioactive molecules from interesting microbes ( Le Goff et al, 2019 ; Nikolaivits et al, 2019 ; Letsiou et al, 2020 ).…”