Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Xuanyu Tao^{1

2

3}, Jiajie Feng^{1

2

3}, Yunfeng Yang⁴, Gangsheng Wang^{1

2

3}, Renmao Tian^{1

2

3}, Fenliang Fan⁵, Daliang Ning^{1

2

3}, Colin T Bates^{1

2

3}, Lauren Hale^{1

2

3}, Mengting M Yuan^{1

2

3}, Linwei Wu^{1

2

3}, Qun Gao⁶, Jiesi Lei⁶, Edward A G Schuur⁷, Julian Yu^{8

9}, Rosvel Bracho¹⁰, Yiqi Luo⁷, Konstantinos T Konstantinidis¹¹, Eric R Johnston¹¹, James R Cole¹², C Ryan Penton^{8

9}, James M Tiedje¹², Jizhong Zhou^{13

14

15

16

17}

Affiliations

¹ Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, 73019, USA.
² Institute for Environmental Genomics, University of Oklahoma, Norman, OK, 73019, USA.
³ School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK, 73019, USA.
⁴ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China. yangyf@tsinghua.edu.cn.
⁵ Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.
⁶ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China.
⁷ Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, 86011, USA.
⁸ College of Integrative Sciences and Arts, Arizona State University, Mesa, AZ, 85212, USA.
⁹ Center for Fundamental and Applied Microbiomics, The Biodesign Institute, Arizona State University, Tempe, AZ, 85281, USA.
¹⁰ School of Forest Resources and Conservation, Department of Biology, University of Florida, Gainesville, FL, 32611, USA.
¹¹ School of Civil and Environmental Engineering, School of Biology, and Center for Bioinformatics and Computational Genomics, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
¹² Center for Microbial Ecology, Michigan State University, East Lansing, MI, 48824, USA.
¹³ Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, 73019, USA. jzhou@ou.edu.
¹⁴ Institute for Environmental Genomics, University of Oklahoma, Norman, OK, 73019, USA. jzhou@ou.edu.
¹⁵ School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK, 73019, USA. jzhou@ou.edu.
¹⁶ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China. jzhou@ou.edu.
¹⁷ Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA. jzhou@ou.edu.

PMID: 32503635
PMCID: PMC7275452
DOI: 10.1186/s40168-020-00838-5

Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Xuanyu Tao et al. Microbiome. 2020.

. 2020 Jun 5;8(1):84.

doi: 10.1186/s40168-020-00838-5.

Authors

Affiliations

¹ Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, 73019, USA.
² Institute for Environmental Genomics, University of Oklahoma, Norman, OK, 73019, USA.
³ School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK, 73019, USA.
⁴ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China. yangyf@tsinghua.edu.cn.
⁵ Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.
⁶ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China.
⁷ Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, 86011, USA.
⁸ College of Integrative Sciences and Arts, Arizona State University, Mesa, AZ, 85212, USA.
⁹ Center for Fundamental and Applied Microbiomics, The Biodesign Institute, Arizona State University, Tempe, AZ, 85281, USA.
¹⁰ School of Forest Resources and Conservation, Department of Biology, University of Florida, Gainesville, FL, 32611, USA.
¹¹ School of Civil and Environmental Engineering, School of Biology, and Center for Bioinformatics and Computational Genomics, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
¹² Center for Microbial Ecology, Michigan State University, East Lansing, MI, 48824, USA.
¹³ Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, 73019, USA. jzhou@ou.edu.
¹⁴ Institute for Environmental Genomics, University of Oklahoma, Norman, OK, 73019, USA. jzhou@ou.edu.
¹⁵ School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK, 73019, USA. jzhou@ou.edu.
¹⁶ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China. jzhou@ou.edu.
¹⁷ Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA. jzhou@ou.edu.

PMID: 32503635
PMCID: PMC7275452
DOI: 10.1186/s40168-020-00838-5

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.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

**Fig. 1**
The absolute abundances of various taxa, measured by 16S rRNA genes, after incubation with ¹³C-vanillin, determined by quantitative polymerase chain reaction (qPCR) and amplicon sequencing. a The numbers of total ¹²C- and ¹³C-labeled 16S rRNA gene copies in ¹³C-vanillin incubated samples (n = 3, biological replicates of warmed or control samples). b The circular maximum likelihood phylogenetic tree of the ¹³C-labeled active decomposer operational taxonomic units (OTUs). Relative abundance is the modified sequence number in heavy fractions (MSNH; see the “Methods” section for details) of the OTU (n = 3, biological replicates of warmed or control samples), c The number of ¹³C-labeled 16S rRNA gene copies of *Burkholderia* (n = 3, biological replicates of warmed or control samples). d The number of ¹³C-labeled 16S rRNA gene copies of α-*Proteobacteria* (n = 3, biological replicates of warmed or control samples). *0.01 < *P ≤* 0.05 and **0.001 < *P ≤* 0.01, as determined by a two-tailed t test. W, warmed soils; C, unwarmed/control soils. Data are shown as mean ± standard error

**Fig. 2**
The accumulated CO₂ flux and the priming effect during the 6-day incubation trial. Red lines/symbols represent in situ warmed soils (W) and blue lines/symbols represent unwarmed/control soils (C). Solid lines represent total CO₂ and dashed lines represent ¹³C-CO₂. The significance of the difference was determined by one-way ANOVA (n = 3, biological replicates of warmed or control samples) on CO₂ amounts and primed C amounts between warmed and control samples (shown in the inset of the figure). W, warmed samples; C, control samples; NS, not significant. Data are shown as mean ± standard error

**Fig. 3**
Normalized signal intensities of key C-decomposing genes in ¹³C-labeled DNA. a Genes associated with aromatic and lignin decomposition. b Aromatics- and lignin-decomposing genes belonging to *Burkholderia* in ¹³C-labeled DNA. c Genes associated with other key C-decomposing pathways. Ppl, phospholipids; Ca, Camphor; Cu, Cutin; and Ta, Terpenes. Differences in relative abundances were determined using one-way ANOVA (n = 3, biological replicates of warmed or control samples). *0.01 < P ≤ 0.05, **0.001 < P ≤ 0.01, and ***P ≤ 0.001. Data are shown as mean ± standard error

**Fig. 4**
Soil and microbial variables simulated by MEND. Warming, in situ warmed soils; Control, unwarmed/control soils. a Simulated and observed soil respiration rates during the 975-day laboratory incubation period, showing high consistency. b Simulated soil heterotrophic respiration rates over 10 years. c Simulated soil organic C over 10 years. d Simulated active microbial biomass C over 10 years. e Simulated decomposition rates of oxidative enzymes over 10 years. The Kruskal-Wallis test was used to determine whether the parameter samples originated from significantly different distribution at a significance level of 0.05

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References

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Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

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Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Authors

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Conflict of interest statement

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