Distinct laccase expression and activity profiles of Trametes versicolor facilitate degradation of benzo[a]pyrene

Yueming Sun; Ying Li; Hong Liang; Ming Li; Ye Liu; Litao Wang; Weijian Lai; Teng Tang; Yongzhao Diao; Yuhong Bai; Christian Isak Jørgensen; Wanghui Xu; Dawen Gao

doi:10.3389/fbioe.2023.1264135

Distinct laccase expression and activity profiles of Trametes versicolor facilitate degradation of benzo[a]pyrene

Front Bioeng Biotechnol. 2023 Sep 21:11:1264135. doi: 10.3389/fbioe.2023.1264135. eCollection 2023.

Authors

Yueming Sun^#¹, Ying Li^#^{2

3}, Hong Liang^{2

3}, Ming Li¹, Ye Liu¹, Litao Wang^{2

3}, Weijian Lai¹, Teng Tang^{2

3}, Yongzhao Diao¹, Yuhong Bai^{2

3}, Christian Isak Jørgensen⁴, Wanghui Xu¹, Dawen Gao^{2

3}

Affiliations

¹ Novozymes (China) Investment Co., Ltd., Beijing, China.
² Centre for Urban Environmental Remediation, Beijing University of Civil Engineering and Architecture, Beijing, China.
³ Beijing Energy Conservation and Sustainable Urban and Rural Development Provincial and Ministry Co-construction Collaboration Innovation Center, Beijing University of Civil Engineering and Architecture, Beijing, China.
⁴ Novozymes A/S, Lyngby, Denmark.

^# Contributed equally.

Abstract

A Trametes versicolor isolate from the Changbai Mountain showed promising activity in degrading benzo[a]pyrene (BaP), which is a high molecular weight (HMW) polycyclic aromatic hydrocarbon (PAH) compound. It was hypothesized that the T. versicolor isolate encode BaP-degrading enzymes, among which laccase is mostly sought after due to significant commercial potential. Genome of the T. versicolor isolate was sequenced and assembled, and seven laccase homologues were identified (TvLac1-7) as candidate genes potentially contributing to BaP degradation. In order to further identify the BaP responsive laccases, time-course transcriptomic and proteomic analyses were conducted in parallel on the T. versicolor isolate upon BaP treatment. Homologous laccases showed distinct expression patterns. Most strikingly, TvLac5 was rapidly induced in the secreted proteomes (secretomes), while TvLac2 was repressed. Recombinant laccase expression and biochemical characterization further showed corresponding enzymatic activity profiles, where TvLac5 was 21-fold more effective in BaP degradation compared to TvLac2. Moreover, TvLac5 also showed 3.6-fold higher BaP degrading activity compared to a commercial laccase product of T. versicolor origin. Therefore, TvLac5 was concluded to be a BaP-responsive enzyme from T. versicolor showing effective BaP degradation activity.

Keywords: Trametes versicolor; benzo[a]pyrene (BaP); laccase; multi-omics; polycyclic aromatic hydrocarbon (PAH); soil remediation.

Grants and funding

The authors declare financial support was received for the research, authorship, and/or publication of this article.The authors gratefully acknowledge the financial support by the National Key R&D Program of the Science and Technology of China (2020YFC1808801).