Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Abstract Background In a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is l...

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Main Authors: Xuanyu Tao, Jiajie Feng, Yunfeng Yang, Gangsheng Wang, Renmao Tian, Fenliang Fan, Daliang Ning, Colin T. Bates, Lauren Hale, Mengting M. Yuan, Linwei Wu, Qun Gao, Jiesi Lei, Edward A. G. Schuur, Julian Yu, Rosvel Bracho, Yiqi Luo, Konstantinos T. Konstantinidis, Eric R. Johnston, James R. Cole, C. Ryan Penton, James M. Tiedje, Jizhong Zhou
Format: Article
Language:English
Published: BMC 2020-06-01
Series:Microbiome
Online Access:http://link.springer.com/article/10.1186/s40168-020-00838-5
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language English
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author Xuanyu Tao
Jiajie Feng
Yunfeng Yang
Gangsheng Wang
Renmao Tian
Fenliang Fan
Daliang Ning
Colin T. Bates
Lauren Hale
Mengting M. Yuan
Linwei Wu
Qun Gao
Jiesi Lei
Edward A. G. Schuur
Julian Yu
Rosvel Bracho
Yiqi Luo
Konstantinos T. Konstantinidis
Eric R. Johnston
James R. Cole
C. Ryan Penton
James M. Tiedje
Jizhong Zhou
spellingShingle Xuanyu Tao
Jiajie Feng
Yunfeng Yang
Gangsheng Wang
Renmao Tian
Fenliang Fan
Daliang Ning
Colin T. Bates
Lauren Hale
Mengting M. Yuan
Linwei Wu
Qun Gao
Jiesi Lei
Edward A. G. Schuur
Julian Yu
Rosvel Bracho
Yiqi Luo
Konstantinos T. Konstantinidis
Eric R. Johnston
James R. Cole
C. Ryan Penton
James M. Tiedje
Jizhong Zhou
Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
Microbiome
author_facet Xuanyu Tao
Jiajie Feng
Yunfeng Yang
Gangsheng Wang
Renmao Tian
Fenliang Fan
Daliang Ning
Colin T. Bates
Lauren Hale
Mengting M. Yuan
Linwei Wu
Qun Gao
Jiesi Lei
Edward A. G. Schuur
Julian Yu
Rosvel Bracho
Yiqi Luo
Konstantinos T. Konstantinidis
Eric R. Johnston
James R. Cole
C. Ryan Penton
James M. Tiedje
Jizhong Zhou
author_sort Xuanyu Tao
title Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
title_short Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
title_full Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
title_fullStr Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
title_full_unstemmed Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
title_sort winter warming in alaska accelerates lignin decomposition contributed by proteobacteria
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2020-06-01
description Abstract Background In a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is limited; thus, it is crucial to identify and evaluate active decomposers of chemically recalcitrant C, which is essential for predicting C-cycle feedbacks and their relative strength of influence on climate change. Using stable isotope probing of the active layer of Arctic tundra soils after depleting soil labile C through a 975-day laboratory incubation, the identity of microbial decomposers of lignin and, their responses to warming were revealed. Results The β-Proteobacteria genus Burkholderia accounted for 95.1% of total abundance of potential lignin decomposers. Consistently, Burkholderia isolated from our tundra soils could grow with lignin as the sole C source. A 2.2 °C increase of warming considerably increased total abundance and functional capacities of all potential lignin decomposers. In addition to Burkholderia, α-Proteobacteria capable of lignin decomposition (e.g. Bradyrhizobium and Methylobacterium genera) were stimulated by warming by 82-fold. Those community changes collectively doubled the priming effect, i.e., decomposition of existing C after fresh C input to soil. Consequently, warming aggravates soil C instability, as verified by microbially enabled climate-C modeling. Conclusions Our findings are alarming, which demonstrate that accelerated C decomposition under warming conditions will make tundra soils a larger biospheric C source than anticipated. Video Abstract
url http://link.springer.com/article/10.1186/s40168-020-00838-5
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spelling doaj-4680458724ab4311bee0f750fabf54b32020-11-25T03:34:21ZengBMCMicrobiome2049-26182020-06-018111210.1186/s40168-020-00838-5Winter warming in Alaska accelerates lignin decomposition contributed by ProteobacteriaXuanyu Tao0Jiajie Feng1Yunfeng Yang2Gangsheng Wang3Renmao Tian4Fenliang Fan5Daliang Ning6Colin T. Bates7Lauren Hale8Mengting M. Yuan9Linwei Wu10Qun Gao11Jiesi Lei12Edward A. G. Schuur13Julian Yu14Rosvel Bracho15Yiqi Luo16Konstantinos T. Konstantinidis17Eric R. Johnston18James R. Cole19C. Ryan Penton20James M. Tiedje21Jizhong Zhou22Department of Microbiology and Plant Biology, University of OklahomaDepartment of Microbiology and Plant Biology, University of OklahomaState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua UniversityDepartment of Microbiology and Plant Biology, University of OklahomaDepartment of Microbiology and Plant Biology, University of OklahomaKey Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesDepartment of Microbiology and Plant Biology, University of OklahomaDepartment of Microbiology and Plant Biology, University of OklahomaDepartment of Microbiology and Plant Biology, University of OklahomaDepartment of Microbiology and Plant Biology, University of OklahomaDepartment of Microbiology and Plant Biology, University of OklahomaState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua UniversityState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua UniversityCenter for Ecosystem Science and Society, Northern Arizona UniversityCollege of Integrative Sciences and Arts, Arizona State UniversitySchool of Forest Resources and Conservation, Department of Biology, University of FloridaCenter for Ecosystem Science and Society, Northern Arizona UniversitySchool of Civil and Environmental Engineering, School of Biology, and Center for Bioinformatics and Computational Genomics, Georgia Institute of TechnologySchool of Civil and Environmental Engineering, School of Biology, and Center for Bioinformatics and Computational Genomics, Georgia Institute of TechnologyCenter for Microbial Ecology, Michigan State UniversityCollege of Integrative Sciences and Arts, Arizona State UniversityCenter for Microbial Ecology, Michigan State UniversityDepartment of Microbiology and Plant Biology, University of OklahomaAbstract Background In a warmer world, microbial decomposition of previously frozen organic carbon (C) is one of the most likely positive climate feedbacks of permafrost regions to the atmosphere. However, mechanistic understanding of microbial mediation on chemically recalcitrant C instability is limited; thus, it is crucial to identify and evaluate active decomposers of chemically recalcitrant C, which is essential for predicting C-cycle feedbacks and their relative strength of influence on climate change. Using stable isotope probing of the active layer of Arctic tundra soils after depleting soil labile C through a 975-day laboratory incubation, the identity of microbial decomposers of lignin and, their responses to warming were revealed. Results The β-Proteobacteria genus Burkholderia accounted for 95.1% of total abundance of potential lignin decomposers. Consistently, Burkholderia isolated from our tundra soils could grow with lignin as the sole C source. A 2.2 °C increase of warming considerably increased total abundance and functional capacities of all potential lignin decomposers. In addition to Burkholderia, α-Proteobacteria capable of lignin decomposition (e.g. Bradyrhizobium and Methylobacterium genera) were stimulated by warming by 82-fold. Those community changes collectively doubled the priming effect, i.e., decomposition of existing C after fresh C input to soil. Consequently, warming aggravates soil C instability, as verified by microbially enabled climate-C modeling. Conclusions Our findings are alarming, which demonstrate that accelerated C decomposition under warming conditions will make tundra soils a larger biospheric C source than anticipated. Video Abstracthttp://link.springer.com/article/10.1186/s40168-020-00838-5