Metagenomic analysis of microbial consortia enriched from compost: new insights into the role of Actinobacteria in lignocellulose decomposition

Abstract

Background: Compost habitats sustain a vast ensemble of microbes specializing in the degradation of lignocellulosic plant materials and are thus important both for their roles in the global carbon cycle and as potential sources of biochemical catalysts for advanced biofuels production. Studies have revealed substantial diversity in compost microbiomes, yet how this diversity relates to functions and even to the genes encoding lignocellulolytic enzymes remains obscure. Here, we used a metagenomic analysis of the rice straw-adapted (RSA) microbial consortia enriched from compost ecosystems to decipher the systematic and functional contexts within such a distinctive microbiome.

Results: Analyses of the 16S pyrotag library and 5 Gbp of metagenomic sequence showed that the phylum Actinobacteria was the predominant group among the Bacteria in the RSA consortia, followed by Proteobacteria, Firmicutes, Chloroflexi, and Bacteroidetes. The CAZymes profile revealed that CAZyme genes in the RSA consortia were also widely distributed within these bacterial phyla. Strikingly, about 46.1 % of CAZyme genes were from actinomycetal communities, which harbored a substantially expanded catalog of the cellobiohydrolase, β-glucosidase, acetyl xylan esterase, arabinofuranosidase, pectin lyase, and ligninase genes. Among these communities, a variety of previously unrecognized species was found, which reveals a greater ecological functional diversity of thermophilic Actinobacteria than previously assumed.

Conclusion: These data underline the pivotal role of thermophilic Actinobacteria in lignocellulose biodegradation processes in the compost habitat. Besides revealing a new benchmark for microbial enzymatic deconstruction of lignocelluloses, the results suggest that actinomycetes found in compost ecosystems are potential candidates for mining efficient lignocellulosic enzymes in the biofuel industry.

Keywords: Actinobacteria; Compost ecosystem; Lignocellulose degradation; Metagenomics.

Fig. 1

Phylogenetic composition of bacterial phyla from environmental gene tags (EGTs) and pyrosequence 16S rDNA sequences from the RSA consortia (a), and network for metagenome taxonomic profiling from the bovine, termite, panda, tammar wallaby samples as well as the RSA consortia (b)

Fig. 2

Distribution pattern of a COG-assigned and b KEGG-assigned proteins in the RSA consortia. Genes not assignable to any COGs or KEGGs are not shown in this figure. The percentage of matched gene numbers was assigned to specific COG or KEGG functional categories

Fig. 3

Phylogenetic distributions of carbohydrate-active enzymes in the most abundant members possessing CAZyme genes. The data were visualized via Circos software [84]. The width of bars from each microbial species and functional enzyme family indicates their relative abundance in the RSA consortia

Fig. 4

An overview of microbial degradation of cellulose and hemicellulose in the RSA consortia. We show the dominant species that digest the cellulose and hemicellulose by depicting the distribution of genes encoding the CAZymes in the RSA consortia. The purple, pink, green, blue, yellow, gray and brown circles represent the members of phylum Actinobacteria, Firmicutes, Proteobacteria, Bacteroidetes, Chloroflexi, Gemmatimonadetes and Crenarchaeota, respectively. The diameter of each circle is proportional to its relative abundance. A. arabaticum, Acetohalobium arabaticum; A. mediterranei, Amycolatopsis mediterranei; A. missouriensis, Actinoplanes missouriensis; A. vinelandii, Azotobacter vinelandii; B. cellulosilyticus, Bacteroides cellulosilyticus; B. cavernae, Beutenbergia cavernae; C. aerophila, Caldilinea aerophila; C. proteoclasticum, Clostridium proteoclasticum; C. flavigena, Cellulomonas flavigena; C. necator, Cupriavidus necator; C. woesei, Conexibacter woesei; D. alkaliphilus, Dethiobacter alkaliphilus; G. aurantiaca, Gemmatimonas aurantiaca; H. aurantiacus, Herpetosiphon aurantiacus; H. orenii, Halothermothrix orenii; K. flavida, Kribbella flavida; M. aurantiaca, Micromonospora aurantiaca; M. australiensis, Mahella australiensis; M. hydrocarbonoclasticus, Marinobacter hydrocarbonoclasticus; M. lupini, Micromonospora lupini; N. hollandicus, Nitrolancetus hollandicus; P. heparinus, Pedobacter heparinus; P. piscicida, Pseudoalteromonas piscicida; P. dioxanivorans, Pseudonocardia dioxanivorans; P. elgii, Paenibacillu elgii; P. maris, Planctomyces maris; P. mucilaginosus, Paenibacillus mucilaginosus; P. suwonensis, Pseudoxanthomonas suwonensis; R. marinus, Rhodothermus marinus; S. bingchenggensis, Streptomyces bingchenggensis; S. clavuligerus, Streptomyces clavuligerus; S. hellenicus, Staphylothermus hellenicus; S. himastatinicus, Streptomyces himastatinicus; S. linguale, Spirosoma linguale; S. nassauensis, Stackebrandtia nassauensis; S. roseum, Streptosporangium roseum; S. scabiei, Streptomyces scabiei; S. thermophilus, Sphaerobacter thermophilus; T. acetatoxydans, Tepidanaerobacter acetatoxydans; T. curvata, Thermomonospora curvata; T. terrenum, Thermobaculum terrenum; T. turnerae, Teredinibacter turnerae; T. bispora, Thermobispora bispora; T. composti, Thermobacillus composti; T. mathranii, Thermoanaerobacter mathranii; T. potens, Thermincola potens; T. thermosaccharolyticum, Thermoanaerobacterium thermosaccharolyticum; V. maris, Verrucosispora maris. The bubble plot indicates the relative abundances of each microbial species in the RSA consortia

Fig. 5

As in Fig. 4 but for microbial degradation of pectin in the RSA consortia