Network analysis and subsequent culturing reveal keystone taxa involved in microbial litter decomposition dynamics

Plant litter decomposition in the soil is governed by microorganisms such as bacteria and fungi that colonize lignocellulose residues during the decomposition process, and thus, the interplay of bacterial and fungal communities can yield insight into the lignocellulose decomposition dynamics. Previo...

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Published inSoil biology & biochemistry Vol. 157; p. 108230
Main Authors Zheng, Haiping, Yang, Tianjie, Bao, Yanzhuo, He, Panpan, Yang, Keming, Mei, Xinlan, Wei, Zhong, Xu, Yangchun, Shen, Qirong, Banerjee, Samiran
Format Journal Article
LanguageEnglish
Published Elsevier Ltd 01.06.2021
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Abstract Plant litter decomposition in the soil is governed by microorganisms such as bacteria and fungi that colonize lignocellulose residues during the decomposition process, and thus, the interplay of bacterial and fungal communities can yield insight into the lignocellulose decomposition dynamics. Previous studies have mainly investigated litter decomposing communities in microcosms or ex-situ conditions or at a single soil ecosystem. Here we conducted a 12 week-long litter decomposition experiment to explore how the temporal dynamics of soil enzyme activities and microbial communities are linked to litter decomposition under three different land use sites (forestland, farmland, and abandoned farmland) in Nanjing, China. We found that litter decomposition in the forestland was the highest among the three land use sites. Then, using a multifactorial approach, we showed that this higher decomposition rate in forest soils is determined by microbial communities with higher ligninolytic enzyme activities, higher diversity, and a less complex but more specialized network. Chryseobacterium in bacteria, and Fusarium, Aspergillus and Penicillium in fungi were the keystone taxa in networks across three land use types. We conducted subsequent culturing that further confirmed the strong decomposition ability and enzyme activities of these taxa, indicating their importance for microbial litter decomposition. As such, this is one of the first studies to validate the role of keystone taxa for litter decomposition, and it demonstrates that co-occurrence network scores can be used for statistical identification of putative keystone taxa for further screening and linking to microbiome functioning. Overall, we show that land use alters the composition and network structure of soil microbiota that determine the litter decomposition. Our study also reveals that specialized keystone taxa are involved in the decomposition dynamics, and highlights an opportunity of harnessing such taxa for manipulating lignocellulose decomposition in soil ecosystems. •Forestland had the highest litter decomposition and lignocellulolytic enzyme activities.•Forestland had greater microbial diversity and a specialized microbial network.•Culturing supported the role of keystone taxa in litter decomposition.
AbstractList Plant litter decomposition in the soil is governed by microorganisms such as bacteria and fungi that colonize lignocellulose residues during the decomposition process, and thus, the interplay of bacterial and fungal communities can yield insight into the lignocellulose decomposition dynamics. Previous studies have mainly investigated litter decomposing communities in microcosms or ex-situ conditions or at a single soil ecosystem. Here we conducted a 12 week-long litter decomposition experiment to explore how the temporal dynamics of soil enzyme activities and microbial communities are linked to litter decomposition under three different land use sites (forestland, farmland, and abandoned farmland) in Nanjing, China. We found that litter decomposition in the forestland was the highest among the three land use sites. Then, using a multifactorial approach, we showed that this higher decomposition rate in forest soils is determined by microbial communities with higher ligninolytic enzyme activities, higher diversity, and a less complex but more specialized network. Chryseobacterium in bacteria, and Fusarium, Aspergillus and Penicillium in fungi were the keystone taxa in networks across three land use types. We conducted subsequent culturing that further confirmed the strong decomposition ability and enzyme activities of these taxa, indicating their importance for microbial litter decomposition. As such, this is one of the first studies to validate the role of keystone taxa for litter decomposition, and it demonstrates that co-occurrence network scores can be used for statistical identification of putative keystone taxa for further screening and linking to microbiome functioning. Overall, we show that land use alters the composition and network structure of soil microbiota that determine the litter decomposition. Our study also reveals that specialized keystone taxa are involved in the decomposition dynamics, and highlights an opportunity of harnessing such taxa for manipulating lignocellulose decomposition in soil ecosystems.
Plant litter decomposition in the soil is governed by microorganisms such as bacteria and fungi that colonize lignocellulose residues during the decomposition process, and thus, the interplay of bacterial and fungal communities can yield insight into the lignocellulose decomposition dynamics. Previous studies have mainly investigated litter decomposing communities in microcosms or ex-situ conditions or at a single soil ecosystem. Here we conducted a 12 week-long litter decomposition experiment to explore how the temporal dynamics of soil enzyme activities and microbial communities are linked to litter decomposition under three different land use sites (forestland, farmland, and abandoned farmland) in Nanjing, China. We found that litter decomposition in the forestland was the highest among the three land use sites. Then, using a multifactorial approach, we showed that this higher decomposition rate in forest soils is determined by microbial communities with higher ligninolytic enzyme activities, higher diversity, and a less complex but more specialized network. Chryseobacterium in bacteria, and Fusarium, Aspergillus and Penicillium in fungi were the keystone taxa in networks across three land use types. We conducted subsequent culturing that further confirmed the strong decomposition ability and enzyme activities of these taxa, indicating their importance for microbial litter decomposition. As such, this is one of the first studies to validate the role of keystone taxa for litter decomposition, and it demonstrates that co-occurrence network scores can be used for statistical identification of putative keystone taxa for further screening and linking to microbiome functioning. Overall, we show that land use alters the composition and network structure of soil microbiota that determine the litter decomposition. Our study also reveals that specialized keystone taxa are involved in the decomposition dynamics, and highlights an opportunity of harnessing such taxa for manipulating lignocellulose decomposition in soil ecosystems. •Forestland had the highest litter decomposition and lignocellulolytic enzyme activities.•Forestland had greater microbial diversity and a specialized microbial network.•Culturing supported the role of keystone taxa in litter decomposition.
ArticleNumber 108230
Author He, Panpan
Shen, Qirong
Mei, Xinlan
Yang, Tianjie
Bao, Yanzhuo
Zheng, Haiping
Wei, Zhong
Xu, Yangchun
Banerjee, Samiran
Yang, Keming
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  givenname: Haiping
  surname: Zheng
  fullname: Zheng, Haiping
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
– sequence: 2
  givenname: Tianjie
  surname: Yang
  fullname: Yang, Tianjie
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
– sequence: 3
  givenname: Yanzhuo
  surname: Bao
  fullname: Bao, Yanzhuo
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
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  givenname: Panpan
  surname: He
  fullname: He, Panpan
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
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  givenname: Keming
  orcidid: 0000-0003-0069-5765
  surname: Yang
  fullname: Yang, Keming
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
– sequence: 6
  givenname: Xinlan
  surname: Mei
  fullname: Mei, Xinlan
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
– sequence: 7
  givenname: Zhong
  surname: Wei
  fullname: Wei, Zhong
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
– sequence: 8
  givenname: Yangchun
  surname: Xu
  fullname: Xu, Yangchun
  email: ycxu@njau.edu.cn
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
– sequence: 9
  givenname: Qirong
  surname: Shen
  fullname: Shen, Qirong
  organization: College of Resources and Environmental Sciences, Jiangsu Provincial Key Laboratory of Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Waste Resource Utilization, Educational Ministry Engineering Center of Resource-saving Fertilizers, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, PR China
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  givenname: Samiran
  surname: Banerjee
  fullname: Banerjee, Samiran
  organization: Department of Microbiological Sciences, North Dakota State University, Fargo, ND, USA
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Network structure
Keystone taxa
Litter decomposition
Microbial community
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Snippet Plant litter decomposition in the soil is governed by microorganisms such as bacteria and fungi that colonize lignocellulose residues during the decomposition...
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StartPage 108230
SubjectTerms abandoned land
agricultural land
Aspergillus
China
Chryseobacterium
Culturing
enzymes
forest land
forests
fungi
Fusarium
Keystone taxa
land use
lignocellulose
Litter decomposition
Microbial community
microbiome
Network structure
Penicillium
plant litter
soil ecosystems
soil enzymes
soil microorganisms
temporal variation
Title Network analysis and subsequent culturing reveal keystone taxa involved in microbial litter decomposition dynamics
URI https://dx.doi.org/10.1016/j.soilbio.2021.108230
https://www.proquest.com/docview/2551961111
Volume 157
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