Genomic Diversity and Phenotypic Variation in Fungal Decomposers Involved in Bioremediation of Persistent Organic Pollutants

Fungi work as decomposers to break down organic carbon, deposit recalcitrant carbon, and transform other elements such as nitrogen. The decomposition of biomass is a key function of wood-decaying basidiomycetes and ascomycetes, which have the potential for the bioremediation of hazardous chemicals present in the environment. Due to their adaptation to different environments, fungal strains have a diverse set of phenotypic traits. This study evaluated 320 basidiomycetes isolates across 74 species for their rate and efficiency of degrading organic dye. We found that dye-decolorization capacity varies among and within species. Among the top rapid dye-decolorizing fungi isolates, we further performed genome-wide gene family analysis and investigated the genomic mechanism for their most capable dye-degradation capacity. Class II peroxidase and DyP-type peroxidase were enriched in the fast-decomposer genomes. Gene families including lignin decomposition genes, reduction-oxidation genes, hydrophobin, and secreted peptidases were expanded in the fast-decomposer species. This work provides new insights into persistent organic pollutant removal by fungal isolates at both phenotypic and genotypic levels.

[1]  Su Sun,et al.  Efficient Azo Dye Biodecolorization System Using Lignin-Co-Cultured White-Rot Fungus , 2023, Journal of fungi.

[2]  Joshua S. Yuan,et al.  Sustainable environmental remediation via biomimetic multifunctional lignocellulosic nano-framework , 2022, Nature Communications.

[3]  B. Henrissat,et al.  The carbohydrate-active enzyme database: functions and literature , 2021, Nucleic Acids Res..

[4]  H. Madhani,et al.  Re-emerging Aspartic Protease Targets: Examining Cryptococcus neoformans Major Aspartyl Peptidase 1 as a Target for Antifungal Drug Discovery , 2021, Journal of medicinal chemistry.

[5]  G. Sciara,et al.  Exploring the Diversity of Fungal DyPs in Mangrove Soils to Produce and Characterize Novel Biocatalysts , 2021, Journal of fungi.

[6]  J. Berrin,et al.  Large-scale phenotyping of 1,000 fungal strains for the degradation of non-natural, industrial compounds , 2021, Communications biology.

[7]  M. Kornaros,et al.  Coupling azo dye degradation and biodiesel production by manganese-dependent peroxidase producing oleaginous yeasts isolated from wood-feeding termite gut symbionts , 2021, Biotechnology for Biofuels.

[8]  B. Henrissat,et al.  Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay , 2021, Environmental microbiology.

[9]  Ben Fulton,et al.  CAFE 5 models variation in evolutionary rates among gene families , 2020, Bioinform..

[10]  Recent Trends in Mycological Research: Volume 2: Environmental and Industrial Perspective , 2021 .

[11]  P. Baldrian,et al.  Ligninolytic Enzyme Production and Decolorization Capacity of Synthetic Dyes by Saprotrophic White Rot, Brown Rot, and Litter Decomposing Basidiomycetes , 2020, Journal of fungi.

[12]  V. R. Murty,et al.  Decolorization of Congo red dye in a continuously operated rotating biological contactor reactor , 2020 .

[13]  S. Sen,et al.  Elucidation of fungal dye‐decolourizing peroxidase (DyP) and ligninolytic enzyme activities in decolourization and mineralization of azo dyes , 2020, Journal of applied microbiology.

[14]  M. Stadler,et al.  Current insights into fungal species diversity and perspective on naming the environmental DNA sequences of fungi , 2019, Mycology.

[15]  W. Schäfer,et al.  Different Hydrophobins of Fusarium graminearum Are Involved in Hyphal Growth, Attachment, Water-Air Interface Penetration and Plant Infection , 2019, Front. Microbiol..

[16]  T. Crowther,et al.  Consistent trade-offs in fungal trait expression across broad spatial scales , 2019, Nature Microbiology.

[17]  S. Kelly,et al.  OrthoFinder: phylogenetic orthology inference for comparative genomics , 2019, Genome Biology.

[18]  D. Hibbett,et al.  Evolutionary dynamics of host specialization in wood-decay fungi , 2018, BMC Evolutionary Biology.

[19]  Jae-Hyuk Yu,et al.  Bioremediation and microbial metabolism of benzo(a)pyrene , 2018, Molecular microbiology.

[20]  F. Assefa,et al.  The Role of Microbial Aspartic Protease Enzyme in Food and Beverage Industries , 2018, Journal of Food Quality.

[21]  Martijn Tennekes,et al.  tmap: Thematic Maps in R , 2018 .

[22]  B. Henrissat,et al.  Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass , 2018, bioRxiv.

[23]  Pratyoosh Shukla,et al.  Contemporary enzyme based technologies for bioremediation: A review. , 2018, Journal of environmental management.

[24]  C. L. Sodré,et al.  Trichosporon asahii secretes a 30-kDa aspartic peptidase. , 2017, Microbiological research.

[25]  D. Hibbett,et al.  A revised family-level classification of the Polyporales (Basidiomycota). , 2017, Fungal biology.

[26]  S. Kelly,et al.  STRIDE: Species Tree Root Inference from Gene Duplication Events , 2017, bioRxiv.

[27]  K. Hyde,et al.  A six-gene phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective , 2017, Fungal Diversity.

[28]  David K. Smith,et al.  ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data , 2017 .

[29]  S. Avery,et al.  Phenotypic heterogeneity in fungi: importance and methodology , 2016 .

[30]  Y. Qu,et al.  Characterization and Strain Improvement of a Hypercellulytic Variant, Trichoderma reesei SN1, by Genetic Engineering for Optimized Cellulase Production in Biomass Conversion Improvement , 2016, Front. Microbiol..

[31]  H. Purohit,et al.  Diverse Metabolic Capacities of Fungi for Bioremediation , 2016, Indian Journal of Microbiology.

[32]  D. Hibbett,et al.  Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities. , 2016, Molecular biology and evolution.

[33]  Joshua S. Yuan,et al.  Genomic and molecular mechanisms for efficient biodegradation of aromatic dye. , 2016, Journal of hazardous materials.

[34]  D. Cullen,et al.  Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood , 2015, Applied and Environmental Microbiology.

[35]  G. Zervakis,et al.  Olive mill wastewater biodegradation potential of white-rot fungi--Mode of action of fungal culture extracts and effects of ligninolytic enzymes. , 2015, Bioresource technology.

[36]  K. Treseder,et al.  Fungal Traits That Drive Ecosystem Dynamics on Land , 2015, Microbiology and Molecular Reviews.

[37]  D. Hibbett,et al.  Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. , 2015, Fungal genetics and biology : FG & B.

[38]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[39]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[40]  Inna Dubchak,et al.  MycoCosm portal: gearing up for 1000 fungal genomes , 2013, Nucleic Acids Res..

[41]  V. Arantes,et al.  Current Understanding of Brown-Rot Fungal Biodegradation Mechanisms: A Review , 2014 .

[42]  M. A. Sanromán,et al.  Feasibility of Solid‐State Fermentation Using Spent Fungi‐Substrate in the Biodegradation of PAHs , 2013 .

[43]  G. R. Jebapriya,et al.  BIOREMEDIATION OF TEXTILE DYE USING WHITE ROT FUNGI: A REVIEW , 2013 .

[44]  Albee Y. Ling,et al.  The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes , 2012, Science.

[45]  J. Latgé,et al.  Hydrophobins—Unique Fungal Proteins , 2012, PLoS pathogens.

[46]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[47]  D. Schlosser,et al.  Untapped potential: exploiting fungi in bioremediation of hazardous chemicals , 2011, Nature Reviews Microbiology.

[48]  A. Meyer,et al.  Juice clarification by protease and pectinase treatments indicates new roles of pectin and protein in cherry juice turbidity , 2010 .

[49]  D. Lindner,et al.  Effects of cloning and root-tip size on observations of fungal ITS sequences from Picea glauca roots , 2009, Mycologia.

[50]  Andrew G. McDonald,et al.  ExplorEnz: the primary source of the IUBMB enzyme list , 2008, Nucleic Acids Res..

[51]  A. L. Santos,et al.  Beneficial Effects of HIV Peptidase Inhibitors on Fonsecaea pedrosoi: Promising Compounds to Arrest Key Fungal Biological Processes and Virulence , 2008, PloS one.

[52]  Kazuya Watanabe,et al.  Microorganisms relevant to bioremediation. , 2001, Current opinion in biotechnology.

[53]  T. Bruns,et al.  ITS primers with enhanced specificity for basidiomycetes ‐ application to the identification of mycorrhizae and rusts , 1993, Molecular ecology.

[54]  T. White Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .