Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment

Yang, Ziming; Yang, Sihang; Van Nostrand, Joy D.; Zhou, Jizhong; Fang, Wei; Qi, Qi; Liu, Yurong; Wullschleger, Stan D.; Liang, Liyuan; Graham, David E.; Yang, Yunfeng; Gu, Baohua

doi:10.3389/fmicb.2017.01741

Title: Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment

Journal Article · Tue Sep 19 00:00:00 EDT 2017 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2017.01741 · OSTI ID:1394250

^[1]; Yang, Sihang ^[2]; Van Nostrand, Joy D. ^[3]; Zhou, Jizhong ^[4]; Fang, Wei ^[5]; Qi, Qi ^[2]; Liu, Yurong ^[6];

^[7]; Liang, Liyuan ^[8];

^[9]; Yang, Yunfeng ^[2];

^[5]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Oakland Univ., Rochester, MI (United States). Dept. of Chemistry
Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment
Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division
Chinese Academy of Sciences (CAS), Beijing (China). Research Center for Eco-Environmental Sciences
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Climate Change Science Inst.
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division

Microbial decomposition of soil organic carbon (SOC) in the thawing Arctic permafrost is one of the most important, but poorly understood, processes in determining the greenhouse gases feedback of tundra ecosystems to climate. Here in this paper, we examine changes in microbial community structure during an anoxic incubation at either –2 or 8 °C for up to 122 days using both an organic and a mineral soil collected from the Barrow Environmental Observatory in northern Alaska, USA. Soils were characterized for SOC chemistry, and GeoChips were used to determine microbial community structure and functional genes associated with C degradation and Fe(III) reduction. We observed notable decreases in functional gene diversity (at P < 0.05) in response to warming at 8 °C, particularly in the organic soil. A number of genes associated with SOC degradation, fermentation, methanogenesis, and iron cycling decreased significantly (P < 0.05) after 122 days of incubation, which coincided well with decreasing labile SOC content, soil respiration, methane production, and iron reduction. The soil type (i.e., organic vs. mineral) and the availability of labile SOC were among the most significant environmental factors impacting the functional community structure. In contrast, the functional structure was largely unchanged in the –2 °C incubation due to low microbial activity resulting in less competition or exclusion. These results demonstrate the vulnerability of SOC in Arctic tundra to warming, facilitated by iron reduction and methanogenesis, and the importance of microbial communities in moderating such vulnerability.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1394250

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 8; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Temperature sensitivity of organic matter decomposition of permafrost-region soils during laboratory incubations Bracho, Rosvel; Natali, Susan; Pegoraro, Elaine Soil Biology and Biochemistry, Vol. 97 https://doi.org/10.1016/j.soilbio.2016.02.008	journal	June 2016
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GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes He, Zhili; Gentry, Terry J.; Schadt, Christopher W. The ISME Journal, Vol. 1, Issue 1 https://doi.org/10.1038/ismej.2007.2	journal	May 2007
The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses Yergeau, Etienne; Hogues, Hervé; Whyte, Lyle G. The ISME Journal, Vol. 4, Issue 9 https://doi.org/10.1038/ismej.2010.41	journal	April 2010
GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity He, Zhili; Deng, Ye; Van Nostrand, Joy D. The ISME Journal, Vol. 4, Issue 9 https://doi.org/10.1038/ismej.2010.46	journal	April 2010
Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments Yergeau, Etienne; Bokhorst, Stef; Kang, Sanghoon The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.124	journal	September 2011
Microbes in thawing permafrost: the unknown variable in the climate change equation Graham, David E.; Wallenstein, Matthew D.; Vishnivetskaya, Tatiana A. The ISME Journal, Vol. 6, Issue 4 https://doi.org/10.1038/ismej.2011.163	journal	November 2011
Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping Zhao, Mengxin; Xue, Kai; Wang, Feng The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.46	journal	April 2014
The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands Yue, Haowei; Wang, Mengmeng; Wang, Shiping The ISME Journal, Vol. 9, Issue 9 https://doi.org/10.1038/ismej.2015.19	journal	February 2015
Forest harvesting reduces the soil metagenomic potential for biomass decomposition Cardenas, Erick; Kranabetter, J. M.; Hope, Graeme The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.57	journal	April 2015
Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships Trivedi, Pankaj; Delgado-Baquerizo, Manuel; Trivedi, Chanda The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.65	journal	May 2016
Nitrogen limitation constrains sustainability of ecosystem response to CO2 Reich, Peter B.; Hobbie, Sarah E.; Lee, Tali Nature, Vol. 440, Issue 7086 https://doi.org/10.1038/nature04486	journal	April 2006
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Davidson, Eric A.; Janssens, Ivan A. Nature, Vol. 440, Issue 7081 https://doi.org/10.1038/nature04514	journal	March 2006
Terrestrial ecosystem carbon dynamics and climate feedbacks Heimann, Martin; Reichstein, Markus Nature, Vol. 451, Issue 7176 https://doi.org/10.1038/nature06591	journal	January 2008
Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M. Nature, Vol. 480, Issue 7377 https://doi.org/10.1038/nature10576	journal	November 2011
Preservation of organic matter in sediments promoted by iron Lalonde, Karine; Mucci, Alfonso; Ouellet, Alexandre Nature, Vol. 483, Issue 7388 https://doi.org/10.1038/nature10855	journal	March 2012
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14238	journal	March 2015
Microbial mediation of carbon-cycle feedbacks to climate warming Zhou, Jizhong; Xue, Kai; Xie, Jianping Nature Climate Change, Vol. 2, Issue 2 https://doi.org/10.1038/nclimate1331	journal	December 2011
Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming Xue, Kai; M. Yuan, Mengting; J. Shi, Zhou Nature Climate Change, Vol. 6, Issue 6 https://doi.org/10.1038/nclimate2940	journal	February 2016
Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands Wang, Chao; Wang, Xiaobo; Liu, Dongwei Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5799	journal	September 2014
High stocks of soil organic carbon in the North American Arctic region Ping, Chien-Lu; Michaelson, Gary J.; Jorgenson, Mark T. Nature Geoscience, Vol. 1, Issue 9 https://doi.org/10.1038/ngeo284	journal	August 2008
Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction Weber, Karrie A.; Achenbach, Laurie A.; Coates, John D. Nature Reviews Microbiology, Vol. 4, Issue 10, p. 752-764 https://doi.org/10.1038/nrmicro1490	journal	October 2006
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