Genomic insights into Penicillium chrysogenum adaptation to subseafloor sedimentary environments

Abstract

Background: Penicillium chrysogenum is a filamentous fungal species with diverse habitats, yet little is known about its genetics in adapting to extreme subseafloor sedimental environments.

Results: Here, we report the discovery of P. chrysogenum strain 28R-6-F01, isolated from deep coal-bearing sediments 2306 m beneath the seafloor. This strain possesses exceptional characteristics, including the ability to thrive in extreme conditions such as high temperature (45 °C), high pressure (35 Mpa), and anaerobic environments, and exhibits broad-spectrum antimicrobial activity, producing the antibiotic penicillin at a concentration of 358 μg/mL. Genome sequencing and assembly revealed a genome size of 33.19 Mb with a GC content of 48.84%, containing 6959 coding genes. Comparative analysis with eight terrestrial strains identified 88 unique genes primarily associated with penicillin and aflatoxins biosynthesis, carbohydrate degradation, viral resistance, and three secondary metabolism gene clusters. Furthermore, significant expansions in gene families related to DNA repair were observed, likely linked to the strain's adaptation to its environmental niche.

Conclusions: Our findings provide insights into the genomic and biological characteristics of P. chrysogenum adaptation to extreme anaerobic subseafloor sedimentary environments, such as high temperature and pressure.

Keywords: Environmental adaptation; Fungi; Penicillium chrysogenum; Secondary metabolites; Subseafloor sediment.

Fig. 1

Colony features of P. chrysogenum 28R-6-F01. A, colony morphology. B, hyphae morphology under optical microscope. C and D, microscopic features of the colonies, hyphae and spores under scanning electron microscope

Fig. 2

Growth of P. chrysogenum 28R-6-F01 in different conditions. A-C, represent the biomass of pressure, temperature, and oxygen, respectively. Error bars indicate standard deviations

Fig. 3

Antimicrobial activity of P. chrysogenum 28R-6-F01. A-D, the inhibitory activity of the fermentation broths on B. subtilis and E. coli, P. capsici and A. sydowii, respectively. 1–3 represent positive control, tested microorganisms, and sterile water, respectively

Fig. 4

The circos diagram of P. chrysogenum 28R-6-F01 genome. The outermost layer is the chromosome and its size. The second layer is GC content, the blue part indicates that the GC content in this area is lower than the whole genome average GC content, and the purple part indicates that the GC content in this area is higher than the whole genome average GC content. The third layer is GC skew (G-C/G + C), the green part indicates that the G content in this area is lower than the C content, and the pink part indicates that the G content in this area is higher than the C content. The fourth to seventh layers are gene density for CDS, rRNA, snRNA, and tRNA, respectively. The eighth layer is the chromosome duplication

Fig. 5

Phylogenetic relationships and gene structure of penicillin biosynthetic genes in different P. chrysogenum strains

Fig. 6

Genome collinearity analysis of P. chrysogenum strains 28R-6-F01 and P2niaD18. The green, and pink box represent the contigs of terrestrial strain P2niaD18, and subseafloor strain 28R-6-F01, respectively. Ligature represent different syntenic blocks

Fig. 7

Phylogenetic tree of the P. chrysogenum and other sequenced filamentous fungi