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Comparative transcriptional analyses of Pleurotus ostreatus mutants on beech wood and rice straw shed light on substrate-biased gene regulation

  • Genomics, transcriptomics, proteomics
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Abstract

Distinct wood degraders occupying their preferred habitats have biased enzyme repertoires that are well fitted to their colonized substrates. Pleurotus ostreatus, commonly found on wood, has evolved its own enzyme-producing traits. In our previous study, transcriptional shifts in several P. ostreatus delignification-defective mutants, including Δhir1 and Δgat1 strains, were analyzed, which revealed the downregulation of ligninolytic genes and the upregulation of cellulolytic and xylanolytic genes when compared to their parental strain 20b on beech wood sawdust medium (BWS). In this study, rice straw (RS) was used as an alternative substrate to examine the transcriptional responses of P. ostreatus to distinct substrates. The vp1 gene and a cupredoxin-encoding gene were significantly upregulated in the 20b strain on RS compared with that on BWS, reflecting their distinct regulation patterns. The overall expression level of genes encoding glucuronidases was also higher on RS than on BWS, showing a good correlation with the substrate composition. Transcriptional alterations in the mutants (Δhir1 or Δgat1 versus 20b strain) on RS were similar to those on BWS, and the extracellular lignocellulose-degrading enzyme activities and lignin-degrading ability of the mutants on RS were consistent with the transcriptional alterations of the corresponding enzyme-encoding genes. However, transcripts of specific genes encoding enzymes belonging to the same CAZyme family exhibited distinct alteration patterns in the mutant strains grown on RS compared to those grown on BWS. These findings provide new insights into the molecular mechanisms underlying the transcriptional regulation of lignocellulolytic genes in P. ostreatus.

Key Points

P. ostreatus expressed variable enzymatic repertoire-related genes in response to distinct substrates.

A demand to upregulate the cellulolytic genes seems to be present in ligninolysis-deficient mutants.

The regulation of some specific genes probably driven by the demand is dependent on the substrate.

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All data supporting the claims of this manuscript are presented and made available in this manuscript.

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Acknowledgments

We would like to thank Prof. Yitzhak Hadar (Hebrew University of Jerusalem, Israel) for providing P. ostreatus strain 20b.

Funding

This work was supported in part by the Institute for Fermentation, Osaka [to T.N.], JSPS KAKENHIs [16K18729 and 19H03017 to T.N.], and the China Scholarship Council [to H.W.].

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Contributions

TN conceived and designed the study. HLW carried out the experiment and drafted the manuscript. HLW, HBX, RHY, DPB and MK performed the analyses, TN, MK, MS, and YH provided editorial suggestions and revisions. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Takehito Nakazawa.

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The authors declare that they have no competing interests.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Wu, H., Nakazawa, T., Xu, H. et al. Comparative transcriptional analyses of Pleurotus ostreatus mutants on beech wood and rice straw shed light on substrate-biased gene regulation. Appl Microbiol Biotechnol 105, 1175–1190 (2021). https://doi.org/10.1007/s00253-020-11087-9

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  • DOI: https://doi.org/10.1007/s00253-020-11087-9

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