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Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting.

ABSTRACT: While decomposition of organic matter by bacteria plays a major role in nutrient cycling in terrestrial ecosystems, the significance of viruses remains poorly understood. Here we combined metagenomics and metatranscriptomics with temporal sampling to study the significance of mesophilic and thermophilic bacteria and their viruses on nutrient cycling during industrial-scale hyperthermophilic composting (HTC). Our results show that virus-bacteria density dynamics and activity are tightly coupled, where viruses specific to mesophilic and thermophilic bacteria track their host densities, triggering microbial community succession via top-down control during HTC. Moreover, viruses specific to mesophilic bacteria encoded and expressed several auxiliary metabolic genes (AMGs) linked to carbon cycling, impacting nutrient turnover alongside bacteria. Nutrient turnover correlated positively with virus-host ratio, indicative of a positive relationship between ecosystem functioning, viral abundances, and viral activity. These effects were predominantly driven by DNA viruses as most detected RNA viruses were associated with eukaryotes and not associated with nutrient cycling during the thermophilic phase of composting. Our findings suggest that DNA viruses could drive nutrient cycling during HTC by recycling bacterial biomass through cell lysis and by expressing key AMGs. Viruses could hence potentially be used as indicators of microbial ecosystem functioning to optimize productivity of biotechnological and agricultural systems.

SUBMITTER: Liao H

PROVIDER: S-EPMC10202948 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting.

Liao Hanpeng H Liu Chen C Ai Chaofan C Gao Tian T Yang Qiu-E QE Yu Zhen Z Gao Shaoming S Zhou Shungui S Friman Ville-Petri VP

The ISME journal 20230408 6

While decomposition of organic matter by bacteria plays a major role in nutrient cycling in terrestrial ecosystems, the significance of viruses remains poorly understood. Here we combined metagenomics and metatranscriptomics with temporal sampling to study the significance of mesophilic and thermophilic bacteria and their viruses on nutrient cycling during industrial-scale hyperthermophilic composting (HTC). Our results show that virus-bacteria density dynamics and activity are tightly coupled, ...[more]

PMID: 37031344

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Project description: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.

Dataset Information

Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting.

Publications

Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting.

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