Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria
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
Affiliations
Xuanyu Tao
Department of Microbiology and Plant Biology, University of Oklahoma
Jiajie Feng
Department of Microbiology and Plant Biology, University of Oklahoma
Yunfeng Yang
State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University
Gangsheng Wang
Department of Microbiology and Plant Biology, University of Oklahoma
Renmao Tian
Department of Microbiology and Plant Biology, University of Oklahoma
Fenliang Fan
Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences
Daliang Ning
Department of Microbiology and Plant Biology, University of Oklahoma
Colin T. Bates
Department of Microbiology and Plant Biology, University of Oklahoma
Lauren Hale
Department of Microbiology and Plant Biology, University of Oklahoma
Mengting M. Yuan
Department of Microbiology and Plant Biology, University of Oklahoma
Linwei Wu
Department of Microbiology and Plant Biology, University of Oklahoma
Qun Gao
State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University
Jiesi Lei
State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University
Edward A. G. Schuur
Center for Ecosystem Science and Society, Northern Arizona University
Julian Yu
College of Integrative Sciences and Arts, Arizona State University
Rosvel Bracho
School of Forest Resources and Conservation, Department of Biology, University of Florida
Yiqi Luo
Center for Ecosystem Science and Society, Northern Arizona University
Konstantinos T. Konstantinidis
School of Civil and Environmental Engineering, School of Biology, and Center for Bioinformatics and Computational Genomics, Georgia Institute of Technology
Eric R. Johnston
School of Civil and Environmental Engineering, School of Biology, and Center for Bioinformatics and Computational Genomics, Georgia Institute of Technology
James R. Cole
Center for Microbial Ecology, Michigan State University
C. Ryan Penton
College of Integrative Sciences and Arts, Arizona State University
James M. Tiedje
Center for Microbial Ecology, Michigan State University
Jizhong Zhou
Department of Microbiology and Plant Biology, University of Oklahoma
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