Abstract
Composting involves the selection of a microbiota capable of resisting the high temperatures generated during the process and degrading the lignocellulose. A deep understanding of the thermophilic microbial community involved in such biotransformation is valuable to improve composting efficiency and to provide thermostable biomass-degrading enzymes for biorefinery. This study investigated the lignocellulose-degrading thermophilic microbial culturome at all the stages of plant waste composting, focusing on the dynamics, enzymes, and thermotolerance of each member of such a community. The results revealed that 58% of holocellulose (cellulose plus hemicellulose) and 7% of lignin were degraded at the end of composting. The whole fungal thermophilic population exhibited lignocellulose-degrading activity, whereas roughly 8–10% of thermophilic bacteria had this trait, although exclusively for hemicellulose degradation (xylan-degrading). Because of the prevalence of both groups, their enzymatic activity, and the wide spectrum of thermotolerance, they play a key role in the breakdown of hemicellulose during the entire process, whereas the degradation of cellulose and lignin is restricted to the activity of a few thermophilic fungi that persists at the end of the process. The xylanolytic bacterial isolates (159 strains) included mostly members of Firmicutes (96%) as well as a few representatives of Actinobacteria (2%) and Proteobacteria (2%). The most prevalent species were Bacillus licheniformis and Aeribacillus pallidus. Thermophilic fungi (27 strains) comprised only four species, namely Thermomyces lanuginosus, Talaromyces thermophilus, Aspergillus fumigatus, and Gibellulopsis nigrescens, of whom A. fumigatus and T. lanuginosus dominated. Several strains of the same species evolved distinctly at the stages of composting showing phenotypes with different thermotolerance and new enzyme expression, even not previously described for the species, as a response to the changing composting environment. Strains of Bacillus thermoamylovorans, Geobacillus thermodenitrificans, T. lanuginosus, and A. fumigatus exhibiting considerable enzyme activities were selected as potential candidates for the production of thermozymes. This study lays a foundation to further investigate the mechanisms of adaptation and acquisition of new traits among thermophilic lignocellulolytic microorganisms during composting as well as their potential utility in biotechnological processing.
Highlights
Lignocellulosic materials, including agricultural and forestry waste, are defined as a valuable renewable carbon resource in the implementation of current biorefineries supported by Circular Economy
Thermophilic microorganisms are not uniquely responsible for the biodegradation of lignocellulose during composting, they play a key role because they actively grow at the thermophilic stage (THER) when it has been reported that lignocellulose degrades at a faster rate (Xiao et al, 2009; Qiao et al, 2019)
Antunes et al (2016), by analyzing the transcriptional profile of genes predicted to be involved in lignocellulose degradation, demonstrated that Lig activity reaches a peak only at the end of the composting, no fungal ligninases (Lacs, manganese peroxidase (MnP), and LIG peroxidase (LiP)) were detected. These results indicate that lignocellulosic biomass deconstruction occurs synergistically and sequentially, FIGURE 4 | Optimal growth temperatures of the thermophilic fungi isolated from compost. (A) Box-and-whisker plot summarizing the range of optimal growth temperature for the different strains of each species; mean values (x), median (I), and outliers ( ) are represented; (B) relative abundance of strains for each species having the optimal growth temperature and enzyme activity: xylanolytic strains with optimal growth at 20◦C (X-20), 30◦C (X-30), 40◦C (X-40), and 50◦C (X-50), and xylanolytic-cellulolytic-ligninolytic strains with optimal growth at 40◦C (XCL-40) and 50◦C (XCL-50)
Summary
Lignocellulosic materials, including agricultural and forestry waste, are defined as a valuable renewable carbon resource in the implementation of current biorefineries supported by Circular Economy. Heat is produced because of the energy generated by exergonic aerobic reactions derived from microbial metabolism This leads the composting to evolve through different stages driven mainly by the temperature reached in the materials being transformed. Based on recent investigations, most microorganisms in composting could be defined as thermotolerant, as they become adapted to the changing temperature of the process (Moreno et al, 2021). These thermotolerant microorganisms are of special interest because of the thermostability of their enzymes (Bhalla et al, 2013), which makes them more competitive in industrial processes, compared to other more thermolabile microorganisms (Hemati et al, 2018)
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