Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils

Abstract Background Microbial-driven decomposition of plant residues is integral to carbon sequestration in terrestrial ecosystems. Actinobacteria, one of the most widely distributed bacterial phyla in soils, are known for their ability to degrade plant residues in vitro. However, their in situ impo...

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Main Authors: Yuanyuan Bao, Jan Dolfing, Zhiying Guo, Ruirui Chen, Meng Wu, Zhongpei Li, Xiangui Lin, Youzhi Feng
Format: Article
Language:English
Published: BMC 2021-04-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-021-01032-x
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spelling doaj-d083735bb7154daabad2f0fa5413d33b2021-04-11T11:40:16ZengBMCMicrobiome2049-26182021-04-019111710.1186/s40168-021-01032-xImportant ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soilsYuanyuan Bao0Jan Dolfing1Zhiying Guo2Ruirui Chen3Meng Wu4Zhongpei Li5Xiangui Lin6Youzhi Feng7State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of SciencesFaculty of Engineering and Environment, Northumbria UniversitySoil Subcenter of Chinese Ecological Research Network, Institute of Soil Science, Chinese Academy of SciencesState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of SciencesState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of SciencesState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of SciencesState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of SciencesState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of SciencesAbstract Background Microbial-driven decomposition of plant residues is integral to carbon sequestration in terrestrial ecosystems. Actinobacteria, one of the most widely distributed bacterial phyla in soils, are known for their ability to degrade plant residues in vitro. However, their in situ importance and specific activity across contrasting ecological environments are not known. Here, we conducted three field experiments with buried straw in combination with microcosm experiments with 13C-straw in paddy soils under different soil fertility levels to reveal the ecophysiological roles of Actinobacteria in plant residue decomposition. Results While accounting for only 4.6% of the total bacterial abundance, the Actinobacteria encoded 16% of total abundance of carbohydrate-active enzymes (CAZymes). The taxonomic and functional compositions of the Actinobacteria were, surprisingly, relatively stable during straw decomposition. Slopes of linear regression models between straw chemical composition and Actinobacterial traits were flatter than those for other taxonomic groups at both local and regional scales due to holding genes encoding for full set of CAZymes, nitrogenases, and antibiotic synthetases. Ecological co-occurrence network and 13C-based metagenomic analyses both indicated that their importance for straw degradation increased in less fertile soils, as both links between Actinobacteria and other community members and relative abundances of their functional genes increased with decreasing soil fertility. Conclusions This study provided DNA-based evidence that non-dominant Actinobacteria plays a key ecophysiological role in plant residue decomposition as their members possess high proportions of CAZymes and as a group maintain a relatively stable presence during plant residue decomposition both in terms of taxonomic composition and functional roles. Their importance for decomposition was more pronounced in less fertile soils where their possession functional genes and interspecies interactions stood out more. Our work provides new ecophysiological angles for the understanding of the importance of Actinobacteria in global carbon cycling. Video abstracthttps://doi.org/10.1186/s40168-021-01032-xActinobacteriaStraw decompositionDNA-SIPShotgun metagenomic sequencingCAZymesSoil fertility
collection DOAJ
language English
format Article
sources DOAJ
author Yuanyuan Bao
Jan Dolfing
Zhiying Guo
Ruirui Chen
Meng Wu
Zhongpei Li
Xiangui Lin
Youzhi Feng
spellingShingle Yuanyuan Bao
Jan Dolfing
Zhiying Guo
Ruirui Chen
Meng Wu
Zhongpei Li
Xiangui Lin
Youzhi Feng
Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils
Microbiome
Actinobacteria
Straw decomposition
DNA-SIP
Shotgun metagenomic sequencing
CAZymes
Soil fertility
author_facet Yuanyuan Bao
Jan Dolfing
Zhiying Guo
Ruirui Chen
Meng Wu
Zhongpei Li
Xiangui Lin
Youzhi Feng
author_sort Yuanyuan Bao
title Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils
title_short Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils
title_full Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils
title_fullStr Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils
title_full_unstemmed Important ecophysiological roles of non-dominant Actinobacteria in plant residue decomposition, especially in less fertile soils
title_sort important ecophysiological roles of non-dominant actinobacteria in plant residue decomposition, especially in less fertile soils
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2021-04-01
description Abstract Background Microbial-driven decomposition of plant residues is integral to carbon sequestration in terrestrial ecosystems. Actinobacteria, one of the most widely distributed bacterial phyla in soils, are known for their ability to degrade plant residues in vitro. However, their in situ importance and specific activity across contrasting ecological environments are not known. Here, we conducted three field experiments with buried straw in combination with microcosm experiments with 13C-straw in paddy soils under different soil fertility levels to reveal the ecophysiological roles of Actinobacteria in plant residue decomposition. Results While accounting for only 4.6% of the total bacterial abundance, the Actinobacteria encoded 16% of total abundance of carbohydrate-active enzymes (CAZymes). The taxonomic and functional compositions of the Actinobacteria were, surprisingly, relatively stable during straw decomposition. Slopes of linear regression models between straw chemical composition and Actinobacterial traits were flatter than those for other taxonomic groups at both local and regional scales due to holding genes encoding for full set of CAZymes, nitrogenases, and antibiotic synthetases. Ecological co-occurrence network and 13C-based metagenomic analyses both indicated that their importance for straw degradation increased in less fertile soils, as both links between Actinobacteria and other community members and relative abundances of their functional genes increased with decreasing soil fertility. Conclusions This study provided DNA-based evidence that non-dominant Actinobacteria plays a key ecophysiological role in plant residue decomposition as their members possess high proportions of CAZymes and as a group maintain a relatively stable presence during plant residue decomposition both in terms of taxonomic composition and functional roles. Their importance for decomposition was more pronounced in less fertile soils where their possession functional genes and interspecies interactions stood out more. Our work provides new ecophysiological angles for the understanding of the importance of Actinobacteria in global carbon cycling. Video abstract
topic Actinobacteria
Straw decomposition
DNA-SIP
Shotgun metagenomic sequencing
CAZymes
Soil fertility
url https://doi.org/10.1186/s40168-021-01032-x
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