Microbial functional diversity covaries with permafrost thaw-induced environmental heterogeneity in tundra soil
Abstract
Permafrost soil in high latitude tundra is one of the largest terrestrial carbon (C) stocks and is highly sensitive to climate warming. Understanding microbial responses to warming-induced environmental changes is critical to evaluating their influences on soil biogeochemical cycles. In this study, a functional gene array (i.e., geochip 4.2) was used to analyze the functional capacities of soil microbial communities collected from a naturally degrading permafrost region in Central Alaska. Varied thaw history was reported to be the main driver of soil and plant differences across a gradient of minimally, moderately, and extensively thawed sites. Compared with the minimally thawed site, the number of detected functional gene probes across the 15-65 cm depth profile at the moderately and extensively thawed sites decreased by 25% and 5%, while the community functional gene β-diversity increased by 34% and 45%, respectively, revealing decreased functional gene richness but increased community heterogeneity along the thaw progression. Particularly, the moderately thawed site contained microbial communities with the highest abundances of many genes involved in prokaryotic C degradation, ammonification, and nitrification processes, but lower abundances of fungal C decomposition and anaerobic-related genes. Significant correlations were observed between functional gene abundance and vascular plant primary productivity, suggesting that plantmore »
- Authors:
-
[1];
[1];
[6];
[1];
- Univ. of Oklahoma, Norman, OK (United States)
- Univ. of Oklahoma, Norman, OK (United States); Univ. of Chinese Academy of Sciences, Beijing (China)
- Univ. of Oklahoma, Norman, OK (United States); Chinese Academy of Sciences (CAS), Beijing (China)
- Univ. of Oklahoma, Norman, OK (United States); East China Normal Univ. (ECNU), Shanghai (China)
- Univ. of Oklahoma, Norman, OK (United States); Central South Univ., Changsha (China)
- Tsinghua Univ., Beijing (China)
- Northern Arizona Univ., Flagstaff, AZ (United States)
- Georgia Inst. of Technology, Atlanta, GA (United States)
- Arizona State Univ., Mesa, AZ (United States)
- Michigan State Univ., East Lansing, MI (United States)
- Univ. of Oklahoma, Norman, OK (United States); Tsinghua Univ., Beijing (China); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1561880
- Alternate Identifier(s):
- OSTI ID: 1415048
- Grant/Contract Number:
- AC02-05CH11231; SC0004601; SC0010715; SC0006982; SC0014085
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Global Change Biology
- Additional Journal Information:
- Journal Volume: 24; Journal Issue: 1; Journal ID: ISSN 1354-1013
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; functional gene array; GEOCHIP; permafrost thaw; soil microbial functional diversity; tussock; tundra
Citation Formats
Yuan, Mengting M., Zhang, Jin, Xue, Kai, Wu, Liyou, Deng, Ye, Deng, Jie, Hale, Lauren, Zhou, Xishu, He, Zhili, Yang, Yunfeng, Van Nostrand, Joy D., Schuur, Edward A. G., Konstantinidis, Konstantinos T., Penton, Christopher R., Cole, James R., Tiedje, James M., Luo, Yiqi, and Zhou, Jizhong. Microbial functional diversity covaries with permafrost thaw-induced environmental heterogeneity in tundra soil. United States: N. p., 2017.
Web. doi:10.1111/gcb.13820.
Yuan, Mengting M., Zhang, Jin, Xue, Kai, Wu, Liyou, Deng, Ye, Deng, Jie, Hale, Lauren, Zhou, Xishu, He, Zhili, Yang, Yunfeng, Van Nostrand, Joy D., Schuur, Edward A. G., Konstantinidis, Konstantinos T., Penton, Christopher R., Cole, James R., Tiedje, James M., Luo, Yiqi, & Zhou, Jizhong. Microbial functional diversity covaries with permafrost thaw-induced environmental heterogeneity in tundra soil. United States. https://doi.org/10.1111/gcb.13820
Yuan, Mengting M., Zhang, Jin, Xue, Kai, Wu, Liyou, Deng, Ye, Deng, Jie, Hale, Lauren, Zhou, Xishu, He, Zhili, Yang, Yunfeng, Van Nostrand, Joy D., Schuur, Edward A. G., Konstantinidis, Konstantinos T., Penton, Christopher R., Cole, James R., Tiedje, James M., Luo, Yiqi, and Zhou, Jizhong. Mon .
"Microbial functional diversity covaries with permafrost thaw-induced environmental heterogeneity in tundra soil". United States. https://doi.org/10.1111/gcb.13820. https://www.osti.gov/servlets/purl/1561880.
@article{osti_1561880,
title = {Microbial functional diversity covaries with permafrost thaw-induced environmental heterogeneity in tundra soil},
author = {Yuan, Mengting M. and Zhang, Jin and Xue, Kai and Wu, Liyou and Deng, Ye and Deng, Jie and Hale, Lauren and Zhou, Xishu and He, Zhili and Yang, Yunfeng and Van Nostrand, Joy D. and Schuur, Edward A. G. and Konstantinidis, Konstantinos T. and Penton, Christopher R. and Cole, James R. and Tiedje, James M. and Luo, Yiqi and Zhou, Jizhong},
abstractNote = {Permafrost soil in high latitude tundra is one of the largest terrestrial carbon (C) stocks and is highly sensitive to climate warming. Understanding microbial responses to warming-induced environmental changes is critical to evaluating their influences on soil biogeochemical cycles. In this study, a functional gene array (i.e., geochip 4.2) was used to analyze the functional capacities of soil microbial communities collected from a naturally degrading permafrost region in Central Alaska. Varied thaw history was reported to be the main driver of soil and plant differences across a gradient of minimally, moderately, and extensively thawed sites. Compared with the minimally thawed site, the number of detected functional gene probes across the 15-65 cm depth profile at the moderately and extensively thawed sites decreased by 25% and 5%, while the community functional gene β-diversity increased by 34% and 45%, respectively, revealing decreased functional gene richness but increased community heterogeneity along the thaw progression. Particularly, the moderately thawed site contained microbial communities with the highest abundances of many genes involved in prokaryotic C degradation, ammonification, and nitrification processes, but lower abundances of fungal C decomposition and anaerobic-related genes. Significant correlations were observed between functional gene abundance and vascular plant primary productivity, suggesting that plant growth and species composition could be co-evolving traits together with microbial community composition. Finally, altogether, this study reveals the complex responses of microbial functional potentials to thaw-related soil and plant changes and provides information on potential microbially mediated biogeochemical cycles in tundra ecosystems.},
doi = {10.1111/gcb.13820},
journal = {Global Change Biology},
number = 1,
volume = 24,
place = {United States},
year = {Mon Jul 17 00:00:00 EDT 2017},
month = {Mon Jul 17 00:00:00 EDT 2017}
}
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Figures / Tables:
Figure 1: (a) Unique and shared probe number detected in the three thawing sites and (b) the categories those unique probes belonged to. Category “others” includes genes gyrB, and those of energy processes, bacteria phages, bioleaching, metal resistance, organic remediation, and virulence categories
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Works referenced in this record:
Dynamics of alpine plant litter decomposition in a changing climate
journal, July 2010
- Gavazov, Konstantin S.
- Plant and Soil, Vol. 337, Issue 1-2
Stochastic Assembly Leads to Alternative Communities with Distinct Functions in a Bioreactor Microbial Community
journal, March 2013
- Zhou, Jizhong; Liu, Wenzong; Deng, Ye
- mBio, Vol. 4, Issue 2
Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest
journal, April 2014
- Taş, Neslihan; Prestat, Emmanuel; McFarland, Jack W.
- The ISME Journal, Vol. 8, Issue 9
Vulnerability of Permafrost Carbon to Climate Change: Implications for the Global Carbon Cycle
journal, September 2008
- Schuur, Edward A. G.; Bockheim, James; Canadell, Josep G.
- BioScience, Vol. 58, Issue 8
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
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
Annual Removal of Aboveground Plant Biomass Alters Soil Microbial Responses to Warming
journal, September 2016
- Xue, Kai; Yuan, Mengting M.; Xie, Jianping
- mBio, Vol. 7, Issue 5
Microbial biogeography: putting microorganisms on the map
journal, February 2006
- Martiny, Jennifer B. Hughes; Bohannan, Brendan J. M.; Brown, James H.
- Nature Reviews Microbiology, Vol. 4, Issue 2
High risk of permafrost thaw
journal, November 2011
- Schuur, Edward A. G.; Abbott, Benjamin
- Nature, Vol. 480, Issue 7375
Climate change and the permafrost carbon feedback
journal, April 2015
- Schuur, E. A. G.; McGuire, A. D.; Schädel, C.
- Nature, Vol. 520, Issue 7546
High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats
journal, January 2015
- Zhou, Jizhong; He, Zhili; Yang, Yunfeng
- mBio, Vol. 6, Issue 1
Response of CO 2 exchange in a tussock tundra ecosystem to permafrost thaw and thermokarst development
journal, January 2009
- Vogel, Jason; Schuur, Edward A. G.; Trucco, Christian
- Journal of Geophysical Research, Vol. 114, Issue G4
Temperature and Plant Species Control Over Litter Decomposition in Alaskan Tundra
journal, February 1996
- Hobbie, Sarah E.
- Ecological Monographs, Vol. 66, Issue 4
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
The interactive effects of soil transplant into colder regions and cropping on soil microbiology and biogeochemistry: Effects of northward soil transplant and cropping
journal, February 2014
- Liu, Shanshan; Wang, Feng; Xue, Kai
- Environmental Microbiology, Vol. 17, Issue 3
Permafrost Degradation and Ecological Changes Associated with a WarmingClimate in Central Alaska
journal, March 2001
- Jorgenson, M. Torre; Racine, Charles H.; Walters, James C.
- Climatic Change, Vol. 48, Issue 4, p. 551-579
Physical and ecological changes associated with warming permafrost and thermokarst in Interior Alaska
journal, July 2009
- Osterkamp, T. E.; Jorgenson, M. T.; Schuur, E. A. G.
- Permafrost and Periglacial Processes, Vol. 20, Issue 3
Holocene Carbon Stocks and Carbon Accumulation Rates Altered in Soils Undergoing Permafrost Thaw
journal, November 2011
- Hicks Pries, Caitlin E.; Schuur, Edward A. G.; Crummer, K. Grace
- Ecosystems, Vol. 15, Issue 1
Stochastic and deterministic assembly processes in subsurface microbial communities
journal, March 2012
- Stegen, James C.; Lin, Xueju; Konopka, Allan E.
- The ISME Journal, Vol. 6, Issue 9
Importance of recent shifts in soil thermal dynamics on growing season length, productivity, and carbon sequestration in terrestrial high-latitude ecosystems
journal, April 2006
- Euskirchen, E. S.; McGUIRE, A. D.; Kicklighter, D. W.
- Global Change Biology, Vol. 12, Issue 4
Biomass offsets little or none of permafrost carbon release from soils, streams, and wildfire: an expert assessment
journal, March 2016
- Abbott, Benjamin W.; Jones, Jeremy B.; Schuur, Edward A. G.
- Environmental Research Letters, Vol. 11, Issue 3
Characteristics of the recent warming of permafrost in Alaska
journal, January 2007
- Osterkamp, T. E.
- Journal of Geophysical Research, Vol. 112, Issue F2
Plant-microbe competition for soil amino acids in the alpine tundra: effects of freeze-thaw and dry-rewet events
journal, January 1998
- Lipson, David A.; Monson, Russell K.
- Oecologia, Vol. 113, Issue 3
The effect of permafrost thaw on old carbon release and net carbon exchange from tundra
journal, May 2009
- Schuur, Edward A. G.; Vogel, Jason G.; Crummer, Kathryn G.
- Nature, Vol. 459, Issue 7246
NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient
journal, November 2016
- Penton, C. Ryan; Yang, Caiyun; Wu, Liyou
- Frontiers in Microbiology, Vol. 7
Expert assessment of vulnerability of permafrost carbon to climate change
journal, March 2013
- Schuur, E. A. G.; Abbott, B. W.; Bowden, W. B.
- Climatic Change, Vol. 119, Issue 2
Multivariate dispersion as a measure of beta diversity
journal, June 2006
- Anderson, Marti J.; Ellingsen, Kari E.; McArdle, Brian H.
- Ecology Letters, Vol. 9, Issue 6
Shifts of tundra bacterial and archaeal communities along a permafrost thaw gradient in Alaska
journal, December 2014
- Deng, Jie; Gu, Yunfu; Zhang, Jin
- Molecular Ecology, Vol. 24, Issue 1
Permafrost thermal state in the polar Northern Hemisphere during the international polar year 2007-2009: a synthesis
journal, April 2010
- Romanovsky, Vladimir E.; Smith, Sharon L.; Christiansen, Hanne H.
- Permafrost and Periglacial Processes, Vol. 21, Issue 2
Stochasticity, succession, and environmental perturbations in a fluidic ecosystem
journal, February 2014
- Zhou, Jizhong; Deng, Ye; Zhang, Ping
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
Global patterns of the isotopic composition of soil and plant nitrogen: GLOBAL SOIL AND PLANT N ISOTOPES
journal, March 2003
- Amundson, Ronald; Austin, A. T.; Schuur, E. A. G.
- Global Biogeochemical Cycles, Vol. 17, Issue 1
Non-parametric multivariate analyses of changes in community structure
journal, March 1993
- Clarke, K. R.
- Austral Ecology, Vol. 18, Issue 1
Microbial ecology and biodiversity in permafrost
journal, March 2006
- Steven, Blaire; Léveillé, Richard; Pollard, Wayne H.
- Extremophiles, Vol. 10, Issue 4
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006
- Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G.
- Annual Review of Plant Biology, Vol. 57, Issue 1
Changes in microbial communities along redox gradients in polygonized Arctic wet tundra soils: Soil microbial communities along a redox gradient
journal, July 2015
- Lipson, David A.; Raab, Theodore K.; Parker, Melanie
- Environmental Microbiology Reports, Vol. 7, Issue 4
Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra: WARMING OF ALASKAN TUNDRA
journal, February 2011
- Natali, Susan M.; Schuur, Edward A. G.; Trucco, Christian
- Global Change Biology, Vol. 17, Issue 3
Plant and Microbe Contribution to Community Resilience in a Directionally Changing Environment
journal, August 2008
- Suding, Katharine N.; Ashton, Isabel W.; Bechtold, Heather
- Ecological Monographs, Vol. 78, Issue 3
Microbial life in permafrost
journal, January 2004
- Rivkina, E.; Laurinavichius, K.; McGrath, J.
- Advances in Space Research, Vol. 33, Issue 8
The microbial ecology of permafrost
journal, May 2014
- Jansson, Janet K.; Taş, Neslihan
- Nature Reviews Microbiology, Vol. 12, Issue 6
Long-term persistence of bacterial DNA
journal, January 2004
- Willerslev, Eske; Hansen, Anders J.; Rønn, Regin
- Current Biology, Vol. 14, Issue 1
Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes
journal, February 1999
- Jonasson, Sven; Michelsen, Anders; Schmidt, Inger K.
- Applied Soil Ecology, Vol. 11, Issue 2-3
Interactions of Bacteria and Fungi on Decomposing Litter: Differential Extracellular Enzyme Activities
journal, October 2006
- Romaní, Anna M.; Fischer, Helmut; Mille-Lindblom, Cecilia
- Ecology, Vol. 87, Issue 10
Role of Land-Surface Changes in Arctic Summer Warming
journal, October 2005
- Chapin, F. S.
- Science, Vol. 310, Issue 5748
Plant Species Composition and Productivity following Permafrost Thaw and Thermokarst in Alaskan Tundra
journal, March 2007
- Schuur, Edward A. G.; Crummer, Kathryn G.; Vogel, Jason G.
- Ecosystems, Vol. 10, Issue 2
Evidence for warming and thawing of discontinuous permafrost in Alaska
journal, January 1999
- Osterkamp, T. E.; Romanovsky, V. E.
- Permafrost and Periglacial Processes, Vol. 10, Issue 1
Microbial seed banks: the ecological and evolutionary implications of dormancy
journal, January 2011
- Lennon, Jay T.; Jones, Stuart E.
- Nature Reviews Microbiology, Vol. 9, Issue 2
Permafrost Meta-Omics and Climate Change
journal, June 2016
- Mackelprang, Rachel; Saleska, Scott R.; Jacobsen, Carsten Suhr
- Annual Review of Earth and Planetary Sciences, Vol. 44, Issue 1
Thawing permafrost increases old soil and autotrophic respiration in tundra: Partitioning ecosystem respiration using δ 13 C and ∆ 14 C
journal, November 2012
- Hicks Pries, Caitlin E.; Schuur, Edward A. G.; Crummer, Kathryn G.
- Global Change Biology, Vol. 19, Issue 2
Understory plant functional groups and litter species identity are stronger drivers of litter decomposition than warming along a boreal forest post-fire successional gradient
journal, July 2016
- De Long, Jonathan R.; Dorrepaal, Ellen; Kardol, Paul
- Soil Biology and Biochemistry, Vol. 98
Redox potential (Eh) and pH as drivers of soil/plant/microorganism systems: a transdisciplinary overview pointing to integrative opportunities for agronomy
journal, September 2012
- Husson, Olivier
- Plant and Soil, Vol. 362, Issue 1-2
Diversity and Evenness: A Unifying Notation and Its Consequences
journal, March 1973
- Hill, M. O.
- Ecology, Vol. 54, Issue 2
Seven-year trends of CO 2 exchange in a tundra ecosystem affected by long-term permafrost thaw : CARBON EXCHANGE IN THAWING TUNDRA
journal, June 2012
- Trucco, Christian; Schuur, Edward A. G.; Natali, Susan M.
- Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G2
Using Mean Similarity Dendrograms to Evaluate Classifications
journal, December 1997
- Sickle, John Van
- Journal of Agricultural, Biological, and Environmental Statistics, Vol. 2, Issue 4
A projection of severe near-surface permafrost degradation during the 21st century
journal, January 2005
- Lawrence, David M.; Slater, Andrew G.
- Geophysical Research Letters, Vol. 32, Issue 24
Bacterial gene abundances as indicators of greenhouse gas emission in soils
journal, February 2010
- Morales, Sergio E.; Cosart, Theodore; Holben, William E.
- The ISME Journal, Vol. 4, Issue 6
The transcriptional response of microbial communities in thawing Alaskan permafrost soils
journal, March 2015
- Coolen, Marco J. L.; Orsi, William D.
- Frontiers in Microbiology, Vol. 6
Microbial responses to southward and northward Cambisol soil transplant
journal, October 2015
- Wang, Mengmeng; Liu, Shanshan; Wang, Feng
- MicrobiologyOpen, Vol. 4, Issue 6
Effects of arctic shrub expansion on biophysical vs. biogeochemical drivers of litter decomposition
journal, July 2014
- DeMarco, Jennie; Mack, Michelle C.; Bret-Harte, M. Syndonia
- Ecology, Vol. 95, Issue 7
Contribution of Stream Detrivores, Fungi, and Bacteria to leaf Breakdown Based on Biomass Estimates
journal, April 2002
- Hieber, Mäggi; Gessner, Mark O.
- Ecology, Vol. 83, Issue 4
The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems
journal, March 2008
- van der Heijden, Marcel G. A.; Bardgett, Richard D.; van Straalen, Nico M.
- Ecology Letters, Vol. 11, Issue 3
Soil organic carbon pools in the northern circumpolar permafrost region: SOIL ORGANIC CARBON POOLS
journal, June 2009
- Tarnocai, C.; Canadell, J. G.; Schuur, E. A. G.
- Global Biogeochemical Cycles, Vol. 23, Issue 2
Soil CO 2 production in upland tundra where permafrost is thawing
journal, January 2010
- Lee, Hanna; Schuur, Edward A. G.; Vogel, Jason G.
- Journal of Geophysical Research, Vol. 115, Issue G1
References
book, January 2012
- Legendre, Pierre; Legendre, Louis
- Developments in Environmental Modelling
GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis
journal, March 2014
- Tu, Qichao; Yu, Hao; He, Zhili
- Molecular Ecology Resources
Molecular investigations into a globally important carbon pool: permafrost-protected carbon in Alaskan soils
journal, February 2010
- Waldrop, M. P.; Wickland, K. P.; White Iii, R.
- Global Change Biology
Works referencing / citing this record:
Biotic responses buffer warming-induced soil organic carbon loss in Arctic tundra
journal, June 2018
- Liang, Junyi; Xia, Jiangyang; Shi, Zheng
- Global Change Biology, Vol. 24, Issue 10
Figures / Tables found in this record:
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.