Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Authors: TAO, XUANYU - University Of Oklahoma; FENG, JIAJIE - University Of Oklahoma; YANG, YUNFEN - Tsinghua University; WANG, GANGSHENG - University Of Oklahoma; TIAN, RENMAO - University Of Oklahoma; FAN, FENLIANG - Chinese Academy Of Agricultural Sciences; NING, DALIANG - University Of Oklahoma; BATES, COLIN - University Of Oklahoma; Hale, Lauren; YUAN, MENGTING - University Of Oklahoma; WU, LINWEI - University Of Oklahoma; GAO, QUN - Tsinghua University; LEI, JIESI - Tsinghua University; SCHUUR, EDWARD - Northern Arizona University; YU, JULIAN - Arizona State University; BRACHO, ROSVEL - University Of Florida; LUO, YIQI - Northern Arizona University; KONSTANTINIDIS, KONSTANTINOS - Georgia Institute Of Technology; JOHNSTON, ERIC - Georgia Institute Of Technology; COLE, JAMES - Michigan State University; PENTON, C - Arizona State University; TIEDJE, JAMES - Michigan State University; ZHOU, JIZHONG - University Of Oklahoma

Submitted to: Microbiome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2020
Publication Date: 6/5/2020
Citation: Tao, X., Feng, J., Yang, Y., Wang, G., Tian, R., Fan, F., Ning, D., Bates, C.T., Hale, L.E., Yuan, M.M., Wu, L., Gao, Q., Lei, J., Schuur, E.A., Yu, J., Bracho, R., Luo, Y., Konstantinidis, K.T., Johnston, E.R., Cole, J.R., Penton, C.R., Tiedje, J.M., Zhou, J. 2020. Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria. Microbiome. 8(1):1-12. https://doi.org/10.1186/s40168-020-00838-5.
DOI: https://doi.org/10.1186/s40168-020-00838-5

Interpretive Summary: Tundra soils comprise a massive quantity of carbon that when thawed could be rapidly decomposed by microorganisms, released as greenhouse gasses, and as such may constitute a positive feedback to climate change. The goal of this work was to gain mechanistic insights into the microbial community responsible for stable/ chemically recalcitrant tundra carbon decomposition. To achieve this, tundra was collected from warmed and non-warmed Alaskan field plots, incubated for 975 days in the lab, then spiked with chemically recalcitrant, isotopically labeled vanillin. Microbial taxa within the phylum Proteobacteria actively decomposed vanillin, which was revealed using both stable isotope probing and DNA sequencing (SIP-seq) and culture-based techniques. Further tundra soils that had experienced warming had a more severe priming effect in response to vanillin substrate addition. These results reveal the vulnerability of tundra soil carbon to temperature changes, as warming stimulated microorganisms within these environments that have capacities to degrade recalcitrant carbon.

Technical 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 ß-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, a-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.