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

Abstract

Microbial decomposition of soil organic carbon (SOC) in thawing Arctic permafrost is important in determining greenhouse gas feedbacks of tundra ecosystems to climate. However, the changes in microbial community structure during SOC decomposition are poorly known. Here we examine these changes using frozen soils from Barrow, Alaska, USA, in anoxic microcosm incubation at -2 and 8°C for 122 days. The functional gene array GeoChip was used to determine microbial community structure and the functional genes associated with SOC degradation, methanogenesis, and Fe(III) reduction. Results show that soil incubation after 122 days at 8°C significantly decreased functional gene abundance (P < 0.05) associated with SOC degradation, fermentation, methanogenesis, and iron cycling, particularly in organic-rich soil. These observations correspond well with decreases in labile SOC content (e.g., reducing sugar and ethanol), methane and CO 2 production, and Fe(III) reduction. In contrast, the community functional structure was largely unchanged in the -2°C incubation. Soil type (i.e., organic vs. mineral) and the availability of labile SOC were among the most significant factors impacting microbial community structure. These results demonstrate the important roles of microbial community in SOC degradation and support previous findings that SOC in organic-rich Arctic tundra is highly vulnerable to microbial degradationmore » under warming.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [2];  [6]; ORCiD logo [7];  [8]; ORCiD logo [9];  [2]; ORCiD logo [5]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Oakland Univ., Rochester, MI (United States). Dept. of Chemistry
  2. Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment
  3. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  4. 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)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division
  6. Chinese Academy of Sciences (CAS), Beijing (China). Research Center for Eco-Environmental Sciences
  7. 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.
  8. 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)
  9. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1394250
Alternate Identifier(s):
OSTI ID: 1416922
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; soil organic carbon; climate warming; microbial community; functional genes; permafrost

Citation Formats

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, and Gu, Baohua. Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01741.
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. Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment. United States. https://doi.org/10.3389/fmicb.2017.01741
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, and Gu, Baohua. Tue . "Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment". United States. https://doi.org/10.3389/fmicb.2017.01741. https://www.osti.gov/servlets/purl/1394250.
@article{osti_1394250,
title = {Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment},
author = {Yang, Ziming and Yang, Sihang and Van Nostrand, Joy D. and Zhou, Jizhong and Fang, Wei and Qi, Qi and Liu, Yurong and Wullschleger, Stan D. and Liang, Liyuan and Graham, David E. and Yang, Yunfeng and Gu, Baohua},
abstractNote = {Microbial decomposition of soil organic carbon (SOC) in thawing Arctic permafrost is important in determining greenhouse gas feedbacks of tundra ecosystems to climate. However, the changes in microbial community structure during SOC decomposition are poorly known. Here we examine these changes using frozen soils from Barrow, Alaska, USA, in anoxic microcosm incubation at -2 and 8°C for 122 days. The functional gene array GeoChip was used to determine microbial community structure and the functional genes associated with SOC degradation, methanogenesis, and Fe(III) reduction. Results show that soil incubation after 122 days at 8°C significantly decreased functional gene abundance (P < 0.05) associated with SOC degradation, fermentation, methanogenesis, and iron cycling, particularly in organic-rich soil. These observations correspond well with decreases in labile SOC content (e.g., reducing sugar and ethanol), methane and CO 2 production, and Fe(III) reduction. In contrast, the community functional structure was largely unchanged in the -2°C incubation. Soil type (i.e., organic vs. mineral) and the availability of labile SOC were among the most significant factors impacting microbial community structure. These results demonstrate the important roles of microbial community in SOC degradation and support previous findings that SOC in organic-rich Arctic tundra is highly vulnerable to microbial degradation under warming.},
doi = {10.3389/fmicb.2017.01741},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Tue Sep 19 00:00:00 EDT 2017},
month = {Tue Sep 19 00:00:00 EDT 2017}
}

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Cited by: 19 works
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Works referenced in this record:

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Development of functional gene microarrays for microbial community analysis
journal, February 2012


Litter, warming and plants affect respiration and allocation of soil microbial and plant C, N and P in arctic mesocosms
journal, July 2004


The temperature dependence of organic-matter decomposition—still a topic of debate
journal, September 2006


Microbial biomass, functional capacity, and community structure after 12 years of soil warming
journal, November 2008


The seasonal pattern of soil microbial community structure in mesic low arctic tundra
journal, October 2013


Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil
journal, April 2016


Temperature sensitivity of organic matter decomposition of permafrost-region soils during laboratory incubations
journal, June 2016


Adsorption and desorption of natural organic matter on iron oxide: mechanisms and models
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Arctic Permafrost Active Layer Detachments Stimulate Microbial Activity and Degradation of Soil Organic Matter
journal, June 2010

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An enzymic 'latch' on a global carbon store
journal, January 2001

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Acclimatization of soil respiration to warming in a tall grass prairie
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GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
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journal, April 2010

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GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity
journal, April 2010


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journal, September 2011

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Microbes in thawing permafrost: the unknown variable in the climate change equation
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Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping
journal, April 2014


The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands
journal, February 2015

  • Yue, Haowei; Wang, Mengmeng; Wang, Shiping
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Forest harvesting reduces the soil metagenomic potential for biomass decomposition
journal, April 2015

  • Cardenas, Erick; Kranabetter, J. M.; Hope, Graeme
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.57

Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships
journal, May 2016

  • Trivedi, Pankaj; Delgado-Baquerizo, Manuel; Trivedi, Chanda
  • The ISME Journal, Vol. 10, Issue 11
  • DOI: 10.1038/ismej.2016.65

Nitrogen limitation constrains sustainability of ecosystem response to CO2
journal, April 2006

  • Reich, Peter B.; Hobbie, Sarah E.; Lee, Tali
  • Nature, Vol. 440, Issue 7086
  • DOI: 10.1038/nature04486

Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
journal, March 2006


Terrestrial ecosystem carbon dynamics and climate feedbacks
journal, January 2008


Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw
journal, November 2011

  • Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M.
  • Nature, Vol. 480, Issue 7377
  • DOI: 10.1038/nature10576

Preservation of organic matter in sediments promoted by iron
journal, March 2012

  • Lalonde, Karine; Mucci, Alfonso; Ouellet, Alexandre
  • Nature, Vol. 483, Issue 7388
  • DOI: 10.1038/nature10855

Microbial mediation of carbon-cycle feedbacks to climate warming
journal, December 2011

  • Zhou, Jizhong; Xue, Kai; Xie, Jianping
  • Nature Climate Change, Vol. 2, Issue 2
  • DOI: 10.1038/nclimate1331

Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming
journal, February 2016

  • Xue, Kai; M. Yuan, Mengting; J. Shi, Zhou
  • Nature Climate Change, Vol. 6, Issue 6
  • DOI: 10.1038/nclimate2940

Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands
journal, September 2014

  • Wang, Chao; Wang, Xiaobo; Liu, Dongwei
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5799

High stocks of soil organic carbon in the North American Arctic region
journal, August 2008

  • Ping, Chien-Lu; Michaelson, Gary J.; Jorgenson, Mark T.
  • Nature Geoscience, Vol. 1, Issue 9
  • DOI: 10.1038/ngeo284

Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction
journal, October 2006

  • Weber, Karrie A.; Achenbach, Laurie A.; Coates, John D.
  • Nature Reviews Microbiology, Vol. 4, Issue 10, p. 752-764
  • DOI: 10.1038/nrmicro1490

One hundred years of Arctic surface temperature variation due to anthropogenic influence
journal, September 2013

  • Fyfe, John C.; von Salzen, Knut; Gillett, Nathan P.
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep02645

Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei
journal, September 2004

  • Holden, M. T. G.; Titball, R. W.; Peacock, S. J.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 39
  • DOI: 10.1073/pnas.0403302101

Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
journal, April 2015

  • Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
  • DOI: 10.1073/pnas.1420797112

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe
journal, August 2015

  • Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 35
  • DOI: 10.1073/pnas.1508382112

Iron oxidation stimulates organic matter decomposition in humid tropical forest soils
journal, July 2013

  • Hall, Steven J.; Silver, Whendee L.
  • Global Change Biology, Vol. 19, Issue 9
  • DOI: 10.1111/gcb.12229

Stoichiometry and temperature sensitivity of methanogenesis and CO 2 production from saturated polygonal tundra in Barrow, Alaska
journal, November 2014

  • Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J.
  • Global Change Biology, Vol. 21, Issue 2
  • DOI: 10.1111/gcb.12762

Poorly crystalline mineral phases protect organic matter in acid subsoil horizons
journal, February 2005


Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem
journal, January 2007


Thermal adaptation of soil microbial respiration to elevated temperature
journal, December 2008


Changes in Ecologically Critical Terrestrial Climate Conditions
journal, August 2013


DNA recovery from soils of diverse composition.
journal, January 1996


Soil bacterial community composition altered by increased nutrient availability in Arctic tundra soils
journal, October 2014

  • Koyama, Akihiro; Wallenstein, Matthew D.; Simpson, Rodney T.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00516

The transcriptional response of microbial communities in thawing Alaskan permafrost soils
journal, March 2015


Water-table height and microtopography control biogeochemical cycling in an Arctic coastal tundra ecosystem
journal, January 2012


Works referencing / citing this record:

Non‐cyanobacterial diazotrophs dominate nitrogen‐fixing communities in permafrost thaw ponds
journal, January 2020

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Biogenic volatile release from permafrost thaw is determined by the soil microbial sink
journal, August 2018


Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes
journal, April 2019

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Impacts of temperature and soil characteristics on methane production and oxidation in Arctic tundra
journal, January 2018

  • Zheng, Jianqiu; RoyChowdhury, Taniya; Yang, Ziming
  • Biogeosciences, Vol. 15, Issue 21
  • DOI: 10.5194/bg-15-6621-2018

Biogenic volatile release from permafrost thaw is determined by the soil microbial sink
journal, August 2018