Unveiling superior phenol detoxification and degradation ability in Candida tropicalis SHC-03: a comparative study with Saccharomyces cerevisiae BY4742

Abstract

This study examined the phenol degradation capabilities and oxidative stress responses of Candida tropicalis SHC-03, demonstrating its metabolic superiority and resilience compared to Saccharomyces cerevisiae BY4742 in a culture medium with phenol as the sole carbon source. Through comparative growth, transcriptomic, and metabolomic analyses under different phenol concentrations, this study revealed C. tropicalis SHC-03's specialized adaptations for thriving in phenol as the sole carbon source environments. These include a strategic shift from carbohydrate metabolism to enhanced phenol degradation pathways, highlighted by the significant upregulation of genes for Phenol 2-monoxygenase and Catechol 1,2-dioxygenase. Despite phenol levels reaching 1.8 g/L, C. tropicalis exhibits a robust oxidative stress response, efficiently managing ROS through antioxidative pathways and the upregulation of genes for peroxisomal proteins like PEX2, PEX13, and PMP34. Concurrently, there was significant upregulation of genes associated with membrane components and transmembrane transporters, enhancing the cell's capacity for substance exchange and signal transduction. Especially, when the phenol concentration was 1.6 g/L and 1.8 g/L, the degradation rates of C. tropicalis towards it were 99.47 and 95.91%, respectively. Conversely, S. cerevisiae BY4742 shows limited metabolic response, with pronounced growth inhibition and lack of phenol degradation. Therefore, our study not only sheds light on the molecular mechanisms underpinning phenol tolerance and degradation in C. tropicalis but also positions this yeast as a promising candidate for environmental and industrial processes aimed at mitigating phenol pollution.

Keywords: Candida tropicalis; Saccharomyces cerevisiae; degradation; phenol; reactive oxygen species.

Figure 1

The growth profiles of C. tropicalis SHC-03 and S. cerevisiae BY4742 in different culture media, as well as the residual phenol concentrations and phenol degradation rates in the culture media. (A) Growth curve of C. tropicalis SHC-03. (B) Growth curve of S. cerevisiae BY4742. (C) Phenol concentration and phenol degradation rate in the culture medium (C. tropicalis SHC-03). (D) Phenol concentration and phenol degradation rate in the culture medium (S. cerevisiae BY4742).

Figure 2

Transcriptome and metabolome analysis of C. tropicalis SHC-03 and S. cerevisiae BY4742. (A) Volcano plot of differentially expressed genes in Saccharomyces cerevisiae BY4742. (B) Volcano plot of differentially expressed genes in C. tropicalis SHC-03. (C) Transcriptionally specific upregulation and downregulation pathways in C. tropicalis SHC-03. (D) Metabolic pathways with specific upregulation and downregulation in C. tropicalis SHC-03. (E) Principal component analysis (PCA) plot of positive metabolites between different samples. (F) Principal component analysis (PCA) plot of negative metabolites between different samples (CK_0h: C. tropicalis SHC-03 0 h; CK_6h: C. tropicalis SHC-03 6 h).

Figure 3

Reactive oxygen species accumulation in C. tropicalis SHC-03 and S. cerevisiae BY4742. (A) Accumulation of reactive oxygen species in cells. (B) The proportion of cells at 1.8 g/L phenol that contained reactive oxygen species after treatment for 0 and 6 h. 2′7′-DCF diacetate (top column): reactive oxygen species indicator dye. DIC (down column): differential interference microscope. Negative: no signal; Positive: there is a signal. * p < 0.05, *** p < 0.001 indicates significant differences. The data represent aver-ages of three experiments. At least 100 cells were examined on each bright-field image.

Figure 4

Differential expression of peroxisome in Candida tropicalis and Saccharomyces cerevisiae.

Figure 5

The first and second step of β-ketoadipate pathway in the biodegradation phenol. Genes significantly upregulated are highlighted in red. The numbers represent transcription levels, quantified as log2 (fold change) of gene expression at 6 h relative to the control at 0 h, indicating the magnitude of upregulation.