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

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GENES AND GENOMES

Exploring the Lignin Catabolism Potential of Soil-Derived Lignocellulolytic Microbial Consortia by a Gene-Centric Metagenomic Approach Laura Díaz-García 1 & Timothy D. H. Bugg 2 & Diego Javier Jiménez 1 Received: 24 March 2020 / Accepted: 15 June 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract An exploration of the ligninolytic potential of lignocellulolytic microbial consortia can improve our understanding of the ecoenzymology 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. A predictive “model” was sketched out, 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 understanding of lignin transformations in soil-derived lignocellulolytic microbial consortia, and pinpointing some bacterial taxa and catabolic genes as ligninolytic trait-markers. Keywords Lignocellulose . Lignin . Metagenomics . Microbial consortia . Soil

Introduction Agricultural residues are an abundant source of sugars used for production of commodity chemicals (e.g., biofuels).

Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01546-1) contains supplementary material, which is available to authorized users. * Diego Javier Jiménez [email protected]; [email protected] 1

Microbiomes and Bioenergy Research Group, Department of Biological Sciences, Universidad de los Andes, Bogotá, Colombia

2

Department of Chemistry, University of Warwick, Coventry, UK

However, the high complexity of plant biomass decreases the saccharification (i.e., release of monosaccharides) rates in biorefineries [1]. This drawback has been att