Salicylic acid is a phenolic phytohormone which controls plant growth and development. A methyl ester (MSA) derivative thereof is volatile and involved in plant-insect or plant-plant communication. Here we show that the nematode-trapping fungus Duddingtonia flagrans uses a methyl-salicylic acid isomer, 6-MSA as morphogen for spatiotemporal control of trap formation and as chemoattractant to lure Caenorhabditis elegans into fungal colonies. 6-MSA is the product of a polyketide synthase and an intermediate in the biosynthesis of arthrosporols. The polyketide synthase (ArtA), produces 6-MSA in hyphal tips, and is uncoupled from other enzymes required for the conversion of 6-MSA to arthrosporols, which are produced in older hyphae. 6-MSA and arthrosporols both block trap formation. The presence of nematodes inhibits 6-MSA and arthrosporol biosyntheses and thereby enables trap formation. 6-MSA and arthrosporols are thus morphogens with some functions similar to quorum-sensing molecules. We show that 6-MSA is important in interkingdom communication between fungi and nematodes.

The hadal biosphere is one of the least understood ecosystems on our planet. Recent studies have revealed diverse and active communities of prokaryotes in hadal sediment. However, there have been few studies on fungi in hadal sediment. Here we report the first isolation and cultivation of 8 fungi from the Mariana Trench sediment. The individual colonies were isolated and identified as Stemphylium sp., Cladosporium sp., Arthrinium sp., Fusarium sp., Alternaria sp., and Aspergillus sp. High hydrostatic pressure (HHP) test was carried out to identify the piezophily of these hadal fungi. Among them, 7 out of the 8 fungal isolates exhibited the ability of germination after incubation under 40 MPa for 7 days. Vegetative growth of the isolates was also affected by HHP. Characterization of secondary metabolites under different pressure conditions was also performed. The production of secondary metabolites was affected by the HHP treatment, improving the potential of discovering novel natural products from hadal fungi. The antibacterial assay revealed the potential of discovering novel natural products. Our results suggest that fungal growth pressure plays an important role in the development and production of secondary metabolites of these hadal fungi under the extreme environment in the Mariana Trench.

Antarctic microbes are important agents for evolutionary adaptation and natural resource of bioactive compounds, harboring the particular metabolic pathways to biosynthesize natural products. However, not much is known on symbiotic microbiomes of fish in the Antarctic zone. In the present study, the culture method and whole-genome sequencing were performed. Natural product analyses were carried out to determine the biosynthetic potential. We report the isolation and identification of a symbiotic bacterium Serratia myotis L7-1, that is highly adaptive and resides within Antarctic fish, Trematomus bernacchii. As revealed by genomic analyses, Antarctic strain S. myotis L7-1 possesses carbohydrate-active enzymes (CAZymes), biosynthetic gene clusters (BGCs), stress response genes, antibiotic resistant genes (ARGs), and a complete type IV secretion system which could facilitate competition and colonization in the extreme Antarctic environment. The identification of microbiome gene clusters indicates the biosynthetic potential of bioactive compounds. Based on bioactivity-guided fractionation, serranticin was purified and identified as the bioactive compound, showing significant antibacterial and antitumor activity. The serranticin gene cluster was identified and located on the chrome. Furthermore, the multidrug resistance and strong bacterial antagonism contribute competitive advantages in ecological niches. Our results highlight the existence of a symbiotic bacterium in Antarctic fish largely represented by bioactive natural products and the adaptability to survive in the fish living in Antarctic oceans.

Deep-sea fungi have evolved extreme environmental adaptation and possess huge biosynthetic potential of bioactive compounds. However, not much is known about the biosynthesis and regulation of secondary metabolites of deep-sea fungi under extreme environments. Here, we presented the isolation of 15 individual fungal strains from the sediments of the Mariana Trench, which were identified by internal transcribed spacer (ITS) sequence analysis as belonging to 8 different fungal species. High hydrostatic pressure (HHP) assays were performed to identify the piezo-tolerance of the hadal fungi. Among these fungi, Aspergillus sydowii SYX6 was selected as the representative due to the excellent tolerance of HHP and biosynthetic potential of antimicrobial compounds. Vegetative growth and sporulation of A. sydowii SYX6 were affected by HHP. Natural product analysis with different pressure conditions was also performed. Based on bioactivity-guided fractionation, diorcinol was purified and characterized as the bioactive compound, showing significant antimicrobial and antitumor activity. The core functional gene associated with the biosynthetic gene cluster (BGC) of diorcinol was identified in A. sydowii SYX6, named as AspksD. The expression of AspksD was apparently regulated by the HHP treatment, correlated with the regulation of diorcinol production. Based on the effect of the HHP tested here, high pressure affected the fungal development and metabolite production, as well as the expression level of biosynthetic genes which revealed the adaptive relationship between the metabolic pathway and the high-pressure environment at the molecular level.

High hydrostatic pressure (HHP) influences the life processes of organisms living at depth in the oceans. While filamentous fungi are one of the essential members of deep-sea microorganisms, few works have explored their piezotolerance to HHP. Here, we obtained three homogeneous Aspergillus sydowii from terrestrial, shallow, and hadal areas, respectively, to compare their pressure resistance. A set of all-around evaluation methods including determination of growth rate, metabolic activity, and microscopic staining observation was established and indicated that A. sydowii DM1 from the hadal area displayed significant piezotolerance. Global analysis of transcriptome data under elevated HHP revealed that A. sydowii DM1 proactively modulated cell membrane permeability, hyphae morphology, and septal quantities for seeking a better livelihood under mild pressure. Besides, differentially expressed genes were mainly enriched in the biosynthesis of amino acids, carbohydrate metabolism, cell process, etc., implying how the filamentous fungi respond to elevated pressure at the molecular level. We speculated that A. sydowii DM1 could acclimatize itself to HHP by adopting several strategies, including environmental response pathway HOG-MAPK, stress proteins, and cellular metabolisms. IMPORTANCE: Fungi play an ecological and biological function in marine environments, while the physiology of filamentous fungi under high hydrostatic pressure (HHP) is an unknown territory due to current technologies. As filamentous fungi are found in various niches, Aspergillus sp. from deep-sea inspire us to the physiological trait of eukaryotes under HHP, which can be considered as a prospective research model. Here, the evaluation methods we constructed would be universal for most filamentous fungi to assess their pressure resistance, and we found that Aspergillus sydowii DM1 from the hadal area owned better piezotolerance and the active metabolisms under HHP indicated the existence of undiscovered metabolic strategies for hadal fungi. Since pressure-related research of marine fungi has been unexpectedly neglected, our study provided an enlightening strategy for them under HHP; we believed that understanding their adaptation and ecological function in original niches will be accelerated in the perceivable future.

The Hadal Zone is acknowledged for its extreme environmental conditions, especially high hydrostatic pressures. The dominant scavengers in the Hadal Zone, Hadal amphipods, fulfill vital roles in the Hadal food web and ecological niches. However, research on the gut microbiota of amphipods related to ecological functions and environmental adaptation is still limited. Here, we used 16S rRNA sequencing technology and a culture-dependent method to analyze the composition of the gut microbiota in Amphipoda living in the Mariana Trench. A total of 16 bacterial genera were identified. Among them, Firmicutes and Proteobacteria were the predominant phyla. The adaptability of gut probiotics to the environment was investigated. Pediococcus pentosaceus XY62 was picked up as the representative strain to elucidate the ecological functions of gut microbes in amphipods. The ProBio database and the K-B agar diffusion method indicated that P. pentosaceus XY62 exhibited the highest probiotic activity compared with all other isolated strains. Specific metabolic pathways and transporter systems that contribute to a range of environmental adaptation strategies have been revealed by genomic analysis of P. pentosaceus XY62. The environmental response genes and a specialized KDP transport system allow it to adapt to the challenging conditions of the Hadal Zone. In addition, the presence of antibacterial compounds and antibiotic resistance genes, as well as the ability to form a biofilm, facilitated the successful colonization of P. pentosaceus XY62 in the gut environment. IMPORTANCE: Amphipods are widely distributed in the Hadal trenches, and the study of their gut microbes has garnered considerable scientific interest. Our research breaks away from traditional omics approaches, innovatively combining sequencing technologies with culture-dependent methods to analyze the gut microbiome structure of amphipods from the Mariana Trench. This not only complements the current omics-dominated field but also paves the way for future resource development of extreme microbes. Furthermore, by conducting genomic analyses and functional validations on a representative strain, we have uncovered its probiotic effects and strategies for adapting to extreme environments. This provides new insights into the theoretical study of the ecological functions of deep-sea bacteria. Overall, our findings offer a fresh perspective on the microbial community structure and environmental adaptation strategies of gut microorganisms in the Hadal Zone.