Metagenomic insights into the development of microbial communities of straw and leaf composts

IntroductionSoil microbiome is a major source of physiologically active microorganisms, which can be potentially mobilized by adding various nutrients. To study this process, a long-term experiment was conducted on the decomposition of oat straw and leaf litter using soil as a microbial inoculum.Met...

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Main Authors: Anastasiia K. Kimeklis, Grigory V. Gladkov, Olga V. Orlova, Tatiana O. Lisina, Alexey M. Afonin, Tatiana S. Aksenova, Arina A. Kichko, Alla L. Lapidus, Evgeny V. Abakumov, Evgeny E. Andronov
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Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1485353/full
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author Anastasiia K. Kimeklis
Anastasiia K. Kimeklis
Grigory V. Gladkov
Olga V. Orlova
Tatiana O. Lisina
Alexey M. Afonin
Alexey M. Afonin
Tatiana S. Aksenova
Arina A. Kichko
Alla L. Lapidus
Evgeny V. Abakumov
Evgeny V. Abakumov
Evgeny E. Andronov
author_facet Anastasiia K. Kimeklis
Anastasiia K. Kimeklis
Grigory V. Gladkov
Olga V. Orlova
Tatiana O. Lisina
Alexey M. Afonin
Alexey M. Afonin
Tatiana S. Aksenova
Arina A. Kichko
Alla L. Lapidus
Evgeny V. Abakumov
Evgeny V. Abakumov
Evgeny E. Andronov
author_sort Anastasiia K. Kimeklis
collection DOAJ
description IntroductionSoil microbiome is a major source of physiologically active microorganisms, which can be potentially mobilized by adding various nutrients. To study this process, a long-term experiment was conducted on the decomposition of oat straw and leaf litter using soil as a microbial inoculum.MethodsCombined analyses of enzymatic activity and NGS data for 16S rRNA gene amplicon and full metagenome sequencing were applied to study taxonomic, carbohydrate-active enzyme (CAZy), and polysaccharide utilization loci (PULs) composition of microbial communities at different stages of decomposition between substrates.ResultsIn straw degradation, the microbial community demonstrated higher amylase, protease, catalase, and cellulase activities, while peroxidase, invertase, and polyphenol oxidase were more active in leaf litter. Consistent with this, the metagenome analysis showed that the microbiome of straw compost was enriched in genes for metabolic pathways of simpler compounds. At the same time, there were more genes for aromatic compound degradation pathways in leaf litter compost. We identified nine metagenome-assembled genomes (MAGs) as the most promising prokaryotic decomposers due to their abnormally high quantity of PULs for their genome sizes, which were confirmed by 16S rRNA gene amplicon sequencing to constitute the bulk of the community at all stages of substrate degradation. MAGs from Bacteroidota (Chitinophaga and Ohtaekwangia) and Actinomycetota (Streptomyces) were found in both composts, while those from Bacillota (Pristimantibacillus) were specific for leaf litter. The most frequently identified PULs were specialized on xylans and pectins, but not cellulose, suggesting that PUL databases may be underrepresented in clusters for complex substrates.DiscussionOur study explores microbial communities from natural ecosystems, such as soil and lignocellulosic waste, which are capable of decomposing lignocellulosic substrates. Using a comprehensive approach with chemical analyses of the substrates, amplicon, and full metagenome sequencing data, we have shown that such communities may be a source of identifying the highly effective decomposing species with novel PULs.
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spelling doaj-art-2209d1e384e54ecaa896a3805081ab5b2025-01-22T07:10:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.14853531485353Metagenomic insights into the development of microbial communities of straw and leaf compostsAnastasiia K. Kimeklis0Anastasiia K. Kimeklis1Grigory V. Gladkov2Olga V. Orlova3Tatiana O. Lisina4Alexey M. Afonin5Alexey M. Afonin6Tatiana S. Aksenova7Arina A. Kichko8Alla L. Lapidus9Evgeny V. Abakumov10Evgeny V. Abakumov11Evgeny E. Andronov12Laboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaDepartment of Applied Ecology, Saint-Petersburg State University, Saint Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaA.I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, Kuopio, FinlandLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaIndependent Researcher, Saint-Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaDepartment of Applied Ecology, Saint-Petersburg State University, Saint Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute of Agricultural Microbiology, Saint Petersburg, RussiaIntroductionSoil microbiome is a major source of physiologically active microorganisms, which can be potentially mobilized by adding various nutrients. To study this process, a long-term experiment was conducted on the decomposition of oat straw and leaf litter using soil as a microbial inoculum.MethodsCombined analyses of enzymatic activity and NGS data for 16S rRNA gene amplicon and full metagenome sequencing were applied to study taxonomic, carbohydrate-active enzyme (CAZy), and polysaccharide utilization loci (PULs) composition of microbial communities at different stages of decomposition between substrates.ResultsIn straw degradation, the microbial community demonstrated higher amylase, protease, catalase, and cellulase activities, while peroxidase, invertase, and polyphenol oxidase were more active in leaf litter. Consistent with this, the metagenome analysis showed that the microbiome of straw compost was enriched in genes for metabolic pathways of simpler compounds. At the same time, there were more genes for aromatic compound degradation pathways in leaf litter compost. We identified nine metagenome-assembled genomes (MAGs) as the most promising prokaryotic decomposers due to their abnormally high quantity of PULs for their genome sizes, which were confirmed by 16S rRNA gene amplicon sequencing to constitute the bulk of the community at all stages of substrate degradation. MAGs from Bacteroidota (Chitinophaga and Ohtaekwangia) and Actinomycetota (Streptomyces) were found in both composts, while those from Bacillota (Pristimantibacillus) were specific for leaf litter. The most frequently identified PULs were specialized on xylans and pectins, but not cellulose, suggesting that PUL databases may be underrepresented in clusters for complex substrates.DiscussionOur study explores microbial communities from natural ecosystems, such as soil and lignocellulosic waste, which are capable of decomposing lignocellulosic substrates. Using a comprehensive approach with chemical analyses of the substrates, amplicon, and full metagenome sequencing data, we have shown that such communities may be a source of identifying the highly effective decomposing species with novel PULs.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1485353/fullstrawleaf littersoil of Chernevaya taigacellulose decompositionPULMAG
spellingShingle Anastasiia K. Kimeklis
Anastasiia K. Kimeklis
Grigory V. Gladkov
Olga V. Orlova
Tatiana O. Lisina
Alexey M. Afonin
Alexey M. Afonin
Tatiana S. Aksenova
Arina A. Kichko
Alla L. Lapidus
Evgeny V. Abakumov
Evgeny V. Abakumov
Evgeny E. Andronov
Metagenomic insights into the development of microbial communities of straw and leaf composts
Frontiers in Microbiology
straw
leaf litter
soil of Chernevaya taiga
cellulose decomposition
PUL
MAG
title Metagenomic insights into the development of microbial communities of straw and leaf composts
title_full Metagenomic insights into the development of microbial communities of straw and leaf composts
title_fullStr Metagenomic insights into the development of microbial communities of straw and leaf composts
title_full_unstemmed Metagenomic insights into the development of microbial communities of straw and leaf composts
title_short Metagenomic insights into the development of microbial communities of straw and leaf composts
title_sort metagenomic insights into the development of microbial communities of straw and leaf composts
topic straw
leaf litter
soil of Chernevaya taiga
cellulose decomposition
PUL
MAG
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1485353/full
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