Taxonomic and functional dynamics of the soil microbiome from a tropical dry forest in kraft lignin-amended microcosms

Abstract

The Caatinga, a Brazilian dry tropical forest that sheds its leaves seasonally, harbors diverse lignocellulose-degrading microbes as a valuable source of lignin-modifying enzymes useful for the chemical and biofuel industry. Nonetheless, the detailed process of lignin decomposition in soils is still poorly understood due to most studies focusing on the biodegradation of non-ligninolytic components of plant biomass (i.e., cellulose, hemicellulose, and oligosaccharides). Hence, the microbial dynamic was investigated in kraft lignin (KL) amended soil microcosms incubated at 45 °C for 9, 18, and 27 days. The changes in the GC-MS profile indicated rapid and complete biodegradation of lignin-derived compounds (i.e., phenol, guaiacol, paracyclophane, eugenol, benzene, ethisterone, and methadone N-oxide) by the microbial ligninolytic systems. Metabarcoding analyses showed that species richness (Chao 1 index from 14313,6 ± 338 to 7230,4 ± 1056) and diversity (H′ index from 7,9 ± 0,05 to 5,6 ± 0,6) decreased in response to KL addition. However, the bacterial diversity was stabilized from the 18th to the 27th day, shaping a soil bacterial community dominated by members of the Proteobacteria (Bordetella and Roseomonas), Firmicutes (Bacillus, Pullulanibacillus, Lysinibacillus, Cohnela, and Ornithinibacilus), and Actinobacteria (Isoptericola, Saccharomonospora, and Beutenbergia) phyla, some of which have not yet been reported as able to degrade lignin. Although the KL addition has promoted the extinction of microbial taxa, the co-occurrence networks reveal high modularity values (0.92) of the microbial structure in the 18th and 27th days of KL-amended soil microcosms, indicating metabolic plasticity even with the ecological disturbance. Some individual taxa clustering into more distinct modules might be explained by the emergence of new ecological niches resulting from the heterogeneous features of KL. Metagenome-based evidence suggests that key bacterial (Bordetella and Streptomyces), and fungal (Aspergillus) members may play synergistic ecophysiological roles in decomposing lignin-derived compounds by carrying the most genes encoding lignin-modifying enzymes belonging to the auxiliary activity (AA) family. The great increase of Aspergillus-affiliated genes of the AA9 family (log ratio of 1.46), which includes the copper-dependent lytic polysaccharide monooxygenases (LPMOs), suggests a key role in lignin-derived compounds degradation. Overall, the insights gathered herein reveal the microbial dynamics of a tropical dry forest soil in kraft lignin-amended microcosms and open perspectives for a rational exploration of potentially novel enzymes and microbial candidates for biotechnological applications.