Functional genomic analysis of bacterial lignin degraders: diversity in mechanisms of lignin oxidation and metabolism

Granja‐Travez, Rommel Santiago; Persinoti, Gabriela Félix; Squina, Fábio M.; Bugg, Timothy D. H.

doi:10.1007/s00253-019-10318-y

Cited by 53 publications

(36 citation statements)

References 80 publications

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“…To date, lignin peroxidase (LiP), versatile peroxidase (VP), manganese peroxidase (MnP), and laccase (Lac) from basidiomycetes and ascomycetes have been well studied, as have lignin-degrading enzymes from basidiomycetes, such as white rot fungi [ 67 , 76 , 77 , 78 ]. In recent years, several DyP-type peroxidases have been found to degrade lignin or its model compounds [ 30 , 79 , 80 , 81 ]. Interestingly, lignin degradation by DyP-type peroxidases has been reported for bacteria as well as basidiomycetes, whereas general lignin-degrading enzymes are mainly isolated from basidiomycetes.…”

Section: Physiological Role Of Dyp-type Peroxidasesmentioning

confidence: 99%

DyP-Type Peroxidases: Recent Advances and Perspectives

Sugano

Yoshida

2021

IJMS

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In this review, we chart the major milestones in the research progress on the DyP-type peroxidase family over the past decade. Though mainly distributed among bacteria and fungi, this family actually exhibits more widespread diversity. Advanced tertiary structural analyses have revealed common and different features among members of this family. Notably, the catalytic cycle for the peroxidase activity of DyP-type peroxidases appears to be different from that of other ubiquitous heme peroxidases. DyP-type peroxidases have also been reported to possess activities in addition to peroxidase function, including hydrolase or oxidase activity. They also show various cellular distributions, functioning not only inside cells but also outside of cells. Some are also cargo proteins of encapsulin. Unique, noteworthy functions include a key role in life-cycle switching in Streptomyces and the operation of an iron transport system in Staphylococcus aureus, Bacillus subtilis and Escherichia coli. We also present several probable physiological roles of DyP-type peroxidases that reflect the widespread distribution and function of these enzymes. Lignin degradation is the most common function attributed to DyP-type peroxidases, but their activity is not high compared with that of standard lignin-degrading enzymes. From an environmental standpoint, degradation of natural antifungal anthraquinone compounds is a specific focus of DyP-type peroxidase research. Considered in its totality, the DyP-type peroxidase family offers a rich source of diverse and attractive materials for research scientists.

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Section: Physiological Role Of Dyp-type Peroxidasesmentioning

confidence: 99%

DyP-Type Peroxidases: Recent Advances and Perspectives

Sugano

Yoshida

2021

IJMS

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“…Its high abundance in the consortia can be correlated with the number of gene copies in Pseudomonas species. For instance, 14 GST genes have been identified in Pseudomonas putida KT2440 [14]. However, not all GST proteins have beta-etherase activity and in-depth functional analysis of these sequences would be worthwhile.…”

Section: Abundance Of Lignin-transforming Enzyme-encoding Genesmentioning

confidence: 99%

“…K15733; EC: 1.11.1.19) involved in bacterial lignin oxidation processes were not identified in the metagenomic annotation, suggesting a low copy numbers within bacterial genomes and/or due to the relative low number of representative sequences available in the KEGG database. In fact, only three genes putative encoding for DyPs has been found in P. fluorescens [46] and around 100 DyPs sequences from bacterial origin are available in a specialized database (http://peroxibase.toulouse.inra.fr/) [14]. As was mentioned, the extracellular depolymerization of lignin releases a mixture of aromatic monomers that can be converted into metabolic intermediates via catechol and protocatechuate pathways.…”

Section: Abundance Of Lignin-transforming Enzyme-encoding Genesmentioning

confidence: 99%

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Exploring the Lignin Catabolism Potential of Soil-Derived Lignocellulolytic Microbial Consortia by a Gene-Centric Metagenomic Approach

2020

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An exploration of the ligninolytic potential of lignocellulolytic microbial consortia can improve our understanding of the eco-enzymology of lignin conversion in nature. In this study, we aimed to detect enriched lignin-transforming enzymes on metagenomes from three soil-derived microbial consortia that were cultivated on "pre-digested" plant biomass (wheat straw -WS1-M, switchgrass -SG-M and corn stover -CS-M). Of 60 selected enzyme-encoding genes putatively involved in lignin catabolism, 20 genes were significantly abundant in WS1-M, CS-M and/or SG-M consortia compared with the initial forest soil inoculum metagenome (FS1). These genes could be involved in lignin oxidation (e.g. superoxide dismutases), oxidative stress responses (e.g. catalase/peroxidases), generation of protocatechuate (e.g. vanAB genes), catabolism of gentisate, catechol and 3phenylpropionic acid (e.g. gentisate 1,2-dioxygenases, muconate cycloisomerases and hcaAB genes), the beta-ketoadipate pathway (e.g. pcaIJ genes) and tolerance to lignocellulose-derived inhibitors (e.g. thymidylate synthases). The taxonomic affiliation of 22 selected lignin-transforming enzymes from WS1-M and CS-M consortia metagenomes revealed that Pseudomonadaceae, Alcaligenaceae, Sphingomonadaceae, Caulobacteraceae, Comamonadaceae and Xanthomonadaceae are the key bacterial families in the catabolism of lignin. We sketched out a predictive "model" where each microbial population has the potential to metabolize an array of aromatic compounds through different pathways, suggesting that lignin catabolism can follow a "task division" strategy.Here, we have established an association between functions and taxonomy, allowing a better 2 understanding of lignin transformations in soil-derived lignocellulolytic microbial consortia, and pinpointing some bacterial taxa and catabolic genes as ligninolytic trait-markers.

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“…Hence it seems likely that hydroxyquinol can be generated from other lignin oxidation reactions involving aryl-C oxidative cleavage of the aryl-C3 unit found in lignin. In a recent survey of the genomes of lignin-degrading bacteria [30], the hydroxyquinol gene cluster was only observed in Rhodococcus jostii RHA1 and Agrobacterium sp., but lignin-degrading Paenibacillus sp. and Ochrobactrum sp.…”

Section: Discussionmentioning

confidence: 99%

The Hydroxyquinol Degradation Pathway in Rhodococcus jostii RHA1 and Agrobacterium Species Is an Alternative Pathway for Degradation of Protocatechuic Acid and Lignin Fragments

Spence

Scott

Dumond

et al. 2020

Appl Environ Microbiol

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Deletion of the pcaHG genes encoding protocatechuate 3,4-dioxygenase in Rhodococcus jostii RHA1 gives a gene deletion strain still able to grow on protocatechuic acid as sole carbon source, indicating a second degradation pathway for protocatechuic acid. Metabolite analysis of wild-type R. jostii RHA1 grown on media containing vanillin or protocatechuic acid indicated the formation of hydroxyquinol (benzene-1,2,4-triol) as a downstream product. Gene cluster ro01857-ro01860 in Rhodococcus jostii RHA1 contains genes encoding hydroxyquinol 1,2-dioxygenase and maleylacetate reductase for degradation of hydroxyquinol but also putative mono-oxygenase (ro01860) and putative decarboxylase (ro01859) genes, and a similar gene cluster is found in the genome of lignin-degrading Agrobacterium sp.. Recombinant R. jostii mono-oxygenase and decarboxylase enzymes were in combination found to convert protocatechuic acid to hydroxyquinol. Hence an alternative pathway for degradation of protocatechuic acid via oxidative decarboxylation to hydroxyquinol is proposed. Importance There is a well-established paradigm for degradation of protocatechuic acid via the β-ketoadipate pathway in a range of soil bacteria. In this study we have found the existence of a second pathway for degradation of protocatechuic acid in Rhodococcus jostii RHA1, via hydroxyquinol (benzene-1,2,4-triol), which establishes a metabolic link between protocatechuic acid and hydroxyquinol. The presence of this pathway in a lignin-degrading Agrobacterium sp. strain suggests a possible involvement of the hydroxyquinol pathway in metabolism of lignin degradation fragments.

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Functional genomic analysis of bacterial lignin degraders: diversity in mechanisms of lignin oxidation and metabolism

Abstract: Please refer to published version for the most recent bibliographic citation information. If a published version is known of, the repository item page linked to above, will contain details on accessing it.

Cited by 53 publications

References 80 publications

DyP-Type Peroxidases: Recent Advances and Perspectives

DyP-Type Peroxidases: Recent Advances and Perspectives

Exploring the Lignin Catabolism Potential of Soil-Derived Lignocellulolytic Microbial Consortia by a Gene-Centric Metagenomic Approach

The Hydroxyquinol Degradation Pathway in Rhodococcus jostii RHA1 and Agrobacterium Species Is an Alternative Pathway for Degradation of Protocatechuic Acid and Lignin Fragments

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