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. 2022 Aug 13;12(9):225. doi: 10.1007/s13205-022-03298-w

RNA-sequencing analysis of bisphenol A biodegradation by white-rot fungus Phanerochaete sordida YK-624

Beijia Wang 1, Jianqiao Wang 1,✉, Ru Yin 1, Xue Zhang 1, Zhonghua Zeng 1, Ge Zhang 1, Nana Wang 1, Hirofumi Hirai 2,3, Tangfu Xiao 1,4
PMCID: PMC9375798  PMID: 35975024

Abstract

Bisphenol A (BPA) is a representative example of an endocrine-disrupting chemical. It is one of the most produced chemical substances in the world, but it causes harmful effects in organisms, such that the effective degradation of BPA is critical. The white-rot fungus Phanerochaete sordida YK-624 has been shown to effectively degrade BPA under ligninolytic and non-ligninolytic conditions. However, it is still unclear what kinds of enzymes are involved in BPA degradation. To explore the mechanism of BPA degradation, the present study analysed the functional genes of P. sordida YK-624 using RNA-sequencing (RNA-Seq). Oxidation–reduction process and metabolic pathway were enriched under ligninolytic and non-ligninolytic conditions by Gene Ontology (GO) analysis and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis. It is suggested that BPA might be used as a carbon source by P. sordida YK-624. Lignin peroxidase and cytochrome P450 were detected in upregulated differentially expressed genes (DEGs). The lignin-degrading enzyme lignin peroxidase and the intracellular cytochrome P450 system were involved in BPA degradation by P. sordida YK-624, respectively. Furthermore, quantitative real-time PCR (qPCR) was used to validate the reliability of the RNA-Seq results.

Supplementary Information

The online version contains supplementary material available at 10.1007/s13205-022-03298-w.

Keywords: Biodegradation, Bisphenol A, Degradation mechanism, Phanerochaete sordida YK-624, RNA-Seq, White-rot fungi

Introduction

Bisphenol A (BPA) is an endocrine-disrupting chemical (EDC) that can produce harmful effects in organisms by interfering with thyroid hormones, estrogen and androgen receptors (De Aguiar Greca et al. 2020; Ejaredar et al. 2017; Zoeller et al. 2005; Ju et al. 2003; Sohoni et al. 2001; Kuiper 1998). BPA is a good chemical additive and has become one of the most commonly used chemicals in the world due to its wide range of applications and increasing demand for plastics. Approximately 95% BPA is used in the production of synthetic polymers, including epoxy resins and polycarbonates (Flint et al. 2012). Many environmental surveys have indicated that BPA is commonly found in surface water, groundwater, wastewater from sewage treatment plants, and landfill leachate (Bhatnagar and Anastopoulos 2017; Zhang et al. 2014). The detected concentration in water environments around the world is also increasing year by year, especially in landfill leachate, and the concentration can even reach 12 mg L−1 (Pedro-Cedillo et al. 2019; Vom Saal 2006). In natural water bodies, the content of BPA is usually at the level of ng·L−1, and that in sediments is usually at the level of ng·g−1 (Jin and Zhu 2016). In addition, the presence of BPA has been detected in various organisms and humans. BPA can disrupt human cell function by interacting with extranuclear receptors, even at low doses measured in ng·L−1 (Michałowicz 2014). BPA not only is an endocrine-disrupting chemical but also causes damage to hepatocytes through oxidative stress (Li et al. 2017; Elswefy et al. 2016; Kourouma et al. 2015). Epidemiological studies have also shown that BPA has a low-dose effect and acts on the body in the form of hormones, thereby affecting the normal endocrine function of the organism and the human body, as well as the development of reproduction, embryos and nervous system, and causing harm to human health and ecology system security (Andújar et al. 2019).

BPA has been limited by some countries and national organizations because of its endocrine-disrupting effects on infants. BPA remains in environmental samples after decades of use (Matsumura et al. 2009; Kitada et al. 2008). In view of the widespread existence and potential harm of BPA, how to control or eliminate BPA pollution has become a hot topic that needs to be resolved in the field of environmental remediation. White-rot fungi are a type of fungi with the most effective ability to degrade lignin to CO2 and H2O in pure culture (Kirk and Farrell 1987). This excellent ability depends on lignin-degrading enzymes, lignin peroxidase (LiP), manganese peroxidase (MnP) and laccase. LiP, the first lignin-degrading enzyme discovered from Phanerochaete chrysosporium, is a glycosylated extracellular haem protein that represents a series of isoenzymes containing Fe3+, a porphyrin ring and a haem group (Tien and Kirk 1988). MnP represents a series of extracellular peroxidases with glycosyl groups. MnP uses the oxidization of two Mn2+ ions to consume one molecule of H2O2, producing two Mn3+ ions (Wong 2009). Laccase was first discovered in 1883 and widely exists in the secretions of many plants and fungi (Mayer and Staples 2002; Yoshida 1883). In recent years, some studies have focused on the biodegradation of BPA by white-rot fungi, such as Stereum hirsutum, Heterobasidium insulare, Phanerochaete chrysosporium, Trametes versicolor, and Pleurotus ostreatus (Grelska and Noszczyńska 2020; Lee et al. 2005). The degradation of BPA by fungi is mainly due to the action of their lignin-degrading enzymes (Jeong-Hun et al. 2006). It was reported that laccase extracted from white-rot fungi could degrade BPA completely within 4 h (Cabana et al. 2007).

The degradation mechanisms of BPA have also been studied. The degradation process of BPA by P. chrysosporium includes the C–C bond breaking between isopropyl and benzene ring, hydroxylation, and demethylation reaction (Wang et al. 2022). The metabolites of degradation of BPA by S. hirsutum and H. insulare were 2-hydroxy-phenylpropionic acid, 4-methoxyphenyl ethene, 2-phenyl acetic acid, and 2-hydroxy-2-phenolacetic acid (Lee et al. 2005). In our previous studies, the white-rot fungus P. sordida YK-624 biodegraded BPA greatly under ligninolytic or non-ligninolytic conditions (Wang et al. 2014, 2013a). BPA dimers are detected as metabolites under ligninolytic conditions by electrospray ionization mass spectrometry (ESI–MS) and nuclear magnetic resonance (NMR) spectroscopy. Under non-ligninolytic conditions, BPA is hydroxylated by P. sordida YK-624 to form hydroxy-BPA, and hydroxy-BPA is further methylated to methoxy-BPA and dimethoxy-BPA.

Previous studies focused on the structural identification of metabolites; however, the degradation mechanism of BPA at the genetic level is not yet understood clearly (Wang et al. 2014, 2013a). In the present study, the functional genes involved in BPA degradation by P. sordida YK-624 were first revealed by RNA sequencing (RNA-Seq) under ligninolytic or non-ligninolytic conditions. The enriched GO term and KEGG pathway were related to oxidation–reduction process and metabolic pathway. The lignin-degrading enzyme LiP and the intracellular cytochrome P450 system were shown to play important roles in BPA degradation by P. sordida YK-624.

Materials and methods

Fungal incubation

The strain P. sordida YK-624 (ATCC 90,872), isolated from rotted wood (Hirai et al. 1994), was grown in potato dextrose agar (PDA) and maintained at 4 ℃. Kirk and potato dextrose broth (PDB) media were used in the degradation experiment. Kirk medium (ligninolytic condition, with the production of ligninolytic enzymes) was prepared according to the method of Kirk et al. (1978). PDB medium (non-ligninolytic condition, non-inducing for production of ligninolytic enzymes) was purchased from Becton, Dickinson and Company.

Transcriptomics analysis and quantitative real-time PCR (qPCR)

The samples were prepared as follows: two sub-cultured P. sordida YK-624 discs were inoculated into 100 mL conical flasks containing 10 mL sterilized Kirk or PDB medium for 3 d static incubation. BPA (Cas number: 80-05-7) was supplied into Kirk and PDB media and incubated at 30 °C at a final concentration of 0.1 mM. The samples were collected according to the results of previous studies, in which those in Kirk medium were incubated for 1 d and those in PDB for 7 d static incubation (Wang et al. 2013a, b). Media lacking BPA were used as a control. Then, fungal mycelia were separated from the solution by suction filtration and stored at -80 ℃. All experiments were performed in triplicate, and all statistical analyses were performed with the Microsoft Office Excel software.

Transcriptomics sample preparation and analysis were described in our previous study (Wang et al. 2021). In brief, RNA was extracted, and the mRNA was purified and fragmented. A cDNA library was constructed, 150 bp paired-end raw reads were generated using an Illumina NovaSeq platform (Parkhomchuk et al. 2009). Then, clean reads were obtained by removing reads containing adapter, reads containing ploy-N and low-quality reads from raw reads. Quality score of 20 (Q20) and Q30 represent every 100 bp or 1000 bp sequencing read may contain an error. The Q20, Q30 and GC content of the clean reads were calculated (Table S3). In the present study, Q20 and Q30 scores were all above 98.2% and 95.2%, shown high accuracy of data were obtained.

Then, the samples without BPA were set as the control, and differential expression analysis was performed. The ligninolytic condition samples for differential expression analysis were described as BPA_K (with BPA) and BPA_K_c (control, without BPA) and BPA_P (with BPA) and BPA_P_c (control, without BPA) for non-ligninolytic conditions. The differentially expressed genes (DEGs) were defined as having a P value < 0.05 and | log2(fold change) |> 1 between BPA-degrading samples and the control. P value and adjust P value (Padj) were used for correcting test of DEGs. DEG functions were annotated based on NCBI non-redundant protein sequences (Nr), Swiss-Prot, Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO). Full lists of DEGs are shown in Table S1 (under ligninolytic conditions) and Table S2 (under non-ligninolytic conditions).

qPCR was performed using an ABI-Viia7 instrument (ABI, America). Reaction solution preparation and PCR amplification reaction were described in our previous studies (Wang et al. 2021). Relative quantification of DEGs expression was determined by 2−ΔΔCT method. Actin was used as a reference gene for normalization, and the primer information used in this research is shown in Table S4.

Results and discussion

Transcriptome analysis under ligninolytic condition

The environmental pollution of BPA is a serious problem, and it can enter the human body through water and food. Numerous studies have demonstrated that white-rot fungi can degrade BPA (Lee et al. 2005; Grelska and Noszczyńska 2020). In our previous study, P. sordida YK-624 could degrade 100% BPA in 1 d under ligninolytic conditions (Wang et al. 2013b). In this study, P. sordida YK-624 was incubated for 1 d after adding BPA, and 100% BPA was degraded (data was shown). Degradation mechanism of BPA at the genetic level has not been studied, RNA-Seq analysis was performed for identifying functional genes in BPA degradation. As shown in Fig. 1a, 137 DEGs were upregulated and 93 genes were downregulated under ligninolytic conditions. However, 68% of the upregulated DEGs were identified as hypothetical protein based on Nr database. Transporter, glycosyltransferase family 8 protein, ricin B-like lectin, pyranose oxidase, fungal hydrophobin were found to be increased at least fourfold in upregulated DEGs (Table S1). Biological importance of transporter is associated with nutrition, defense, and detoxification (Diallinas 2016). Ricin B-like lectin is important mediator in fungal defense (Žurga et al. 2015). The addition of BPA might be caused fungal defense to degrade BPA for their detoxification. Pyranose oxidase is a source of H2O2 for the activity of ligninolytic peroxidases (Daniel et al. 1994). Some peroxidases have been reported that they could effectively remove BPA, such as horseradish peroxidase, soybean peroxidase, and lignin-degrading enzymes LiP and MnP (Hirano et al. 2000; Kimura et al. 2004; Sakuyama et al. 2003; Watanabe et al. 2011). The ligninolytic enzyme laccase was also reported to degrade BPA (Tsutsumi et al. 2001; Zeng et al. 2017). After Coriolopsis gallica laccase treatment for 4 h, the amount of BPA was decreased by 100% (Daâssi et al. 2016). In the present study, LiP was identified in upregulated DEGs, but MnP was not found in this study (Table S1).

Fig. 1.

Fig. 1

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Volcano plot of differentially expressed genes (DEGs) of Phanerochaete sordida YK-624. a BPA_K (with BPA) versus BPA_K_c (without BPA) for ligninolytic condition; b BPA_P (with BPA) versus BPA_P_c (without BPA) for non-ligninolytic condition. Red plot: upregulated genes; green plot: downregulated genes; blue plot: nonsignificant genes

To further explore the DEGs, we performed GO function and KEGG pathway analysis. GO analysis of upregulated DEGs under ligninolytic conditions indicated that “oxidation–reduction process” was enriched in the biological process category, while “coenzyme binding” was enriched in the molecular function category. Tryptophan metabolism and fatty acid degradation were the most enriched KEGG pathways (Fig. 2a). These results suggested that oxidation–reduction enzymes might play an important role in BPA degradation by P. sordida YK-624 under ligninolytic condition.

Fig. 2.

Fig. 2

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Gene ontology (GO) classification of upregulated genes involved in BPA degradation under non-ligninolytic condition. Blue: molecular function (MF) categories; red: biological process (BP) categories

Transcriptome analysis under non-ligninolytic condition

In our previous study, P. sordida YK-624 could degrade 83% BPA under non-ligninolytic conditions after 7 d of incubation (Wang et al. 2013a). Three BPA metabolites were detected, but the function genes in BPA degradation were not yet understood clearly. The samples preparation for RNA-Seq analysis were based on our previous results, and incubation without BPA was the control. Under non-ligninolytic conditions, 148 DEGs were upregulated, and 157 genes were downregulated (Fig. 1b). However, 78% of the upregulated DEGs were identified as hypothetical protein based on Nr database (Table S2). Two genes coding for medium-chain dehydrogenase/reductase like protein were identified in upregulated DEGs with 106- and 57-fold increased. A large of enzymes belongs to the medium-chain dehydrogenase/reductase superfamily, a broad range of activities have reported (Tiwari et al. 2012). It might be involved in the intracellular degradation of BPA.

According to the GO function and KEGG pathway analysis, “oxidation–reduction process”, “single-organism metabolic process” and “generation of precursor metabolites and energy” were the top three significantly enriched terms in the biological process category for the upregulated DEGs under non-ligninolytic conditions (Fig. 3). “Oxidoreductase activity”, “heme binding”, and “tetrapyrrole binding” were the most significantly enriched terms in the molecular function category under non-ligninolytic conditions (Fig. 3). Mechanism related pathways were mostly identified in the KEGG pathway of upregulated DEGs (Fig. 2b). Microbial biotransformation of various pollutants and xenobiotic compounds occurs through oxidation, reduction, hydrolysis and so on. (Smitha et al. 2017). In addition to these extracellular enzymes, the intracellular cytochrome P450 system was identified to be involved in BPA degradation (Husain and Qayyum 2013; Jia et al. 2020). Cytochromes P450 in white-rot fungi have been observed to degrade various recalcitrant aromatic compounds (Ichinose 2013; Wang et al. 2019; Xiao and Kondo 2019).

Fig. 3.

Fig. 3

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Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway classification of upregulated differentially expressed genes (DEGs) involved in BPA degradation by P. sordida YK-624. a Ligninolytic condition; b non-ligninolytic condition. ABC transporters ATP-binding cassette transporter

Degradation mechanism of BPA

Degradation mechanisms of BPA by microorganism have been widely reported. Bacteria-mediated bisphenol A degradation was summarized by Zhang et al. 2013. White-rot fungus P. chrysosporium could degrade BPA through the C–C bond breaking between isopropyl and benzene ring, hydroxylation, and demethylation reaction (Wang et al. 2022). The metabolites of degradation of BPA by S. hirsutum and H. insulare were 2-hydroxy-phenylpropionic acid, 4-methoxyphenyl ethene, 2-phenyl acetic acid, and 2-hydroxy-2-phenolacetic acid (Lee et al. 2005). Transcriptome analysis of BPA degradation by Desmodesmus sp.WR1 showed that algae significantly upregulated oxidoreductase-encoding genes for BPA degradation (Wang et al. 2017).

P. sordida YK-624 is isolated from rotted wood in Japan, has excellent lignin-degrading activity than model white-rot fungus (Hirai et al. 1994). P. sordida YK-624 can degrade a wide range of organic pollutants, such as dibenzo-p-dioxins, aflatoxin B1, EDCs, and neonicotinoid pesticides (Takada et al. 1996; Wang et al. 2011, 2012b, 2013a, 2014, 2019). Our previous results found that LiP of P. sordida YK-624 could completely degrade BPA (Wang et al. 2012a), and the metabolite BPA dimers were identified (Wang et al. 2013b). Under non-ligninolytic conditions, BPA is hydroxylated by P. sordida YK-624 to form hydroxy-BPA, and hydroxy-BPA is further methylated to methoxy-BPA and dimethoxy-BPA (Wang et al. 2014). The estrogenic activities of these metabolites of BPA were much lower than that of BPA, cytochromes P450s and O-methyltransferase might be involved in BPA degradation by P. sordida YK-624 (Wang et al. 2014). In our recent study, transcriptomic analysis results of bisphenol F degradation by P. sordida YK-624 indicated that LiP and MnP are important for BPF degradation and cytochrome P450s play a small role (Wang et al. 2021). In the present study, four cytochromes P450s and one methyltransferase were identified in upregulated DEGs (Table S2). This result is consistent with our previous study, which suggested that cytochrome P450 and methyltransferase were involved in BPA degradation.

QPCR analysis

To validate the reliability of the expression profiles obtained from RNA-Seq, the expression levels of upregulated DEGs in BPA degradation by P. sordida YK-624 were compared by qPCR. The trends of the expression of these DEGs were similar to the RNA-Seq results (Fig. S1).

Conclusions

In summary, the present study analyzed the functional genes of P. sordida YK-624 in BPA degradation by RNA-Seq. Two conditions, ligninolytic and non-ligninolytic, were used to study the degradation mechanism. The lignin-degrading enzyme LiP and the intracellular cytochrome P450 system might play important roles in BPA degradation by P. sordida YK-624 under ligninolytic and non-ligninolytic conditions, respectively. The results of this study provide a better understanding of BPA degradation at the genetic level by white-rot fungi. However, approximately 70% of hypothetical proteins were identified in upregulated DEGs, and these DEGs need to be further explored in depth.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 150 KB) (150.3KB, docx)

Author contributions

JW, BW, and TX developed the idea of the study, participated in its design and coordination and helped to draft the manuscript. RY, XZ, ZZ, GZ and NW contributed to the acquisition and interpretation of data. HH provided critical review and substantially revised the manuscript. All authors read and approved the final manuscript.

Funding

The work was financially supported by the Science and Technology Program of Guangzhou, China (no. 202002030090).

Availability of data and materials

The data sets supporting the results of this article are available in NCBI (accession numbers for the sequences of P. sordida YK-624 are SUB9742279 under ligninolytic condition and SUB9742382 under non-ligninolytic condition, respectively).

Declarations

Conflict of interest

The authors declare that they have no conflict of interest in the publication.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary file1 (DOCX 150 KB) (150.3KB, docx)

Data Availability Statement

The data sets supporting the results of this article are available in NCBI (accession numbers for the sequences of P. sordida YK-624 are SUB9742279 under ligninolytic condition and SUB9742382 under non-ligninolytic condition, respectively).

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