Winter warming rapidly increases carbon degradation capacities of fungal communities in tundra soil: Potential consequences on carbon stability
Abstract
We report high-latitude tundra ecosystems are increasingly affected by climate warming. As an important fraction of soil microorganisms, fungi play essential roles in carbon degradation, especially the old, chemically recalcitrant carbon. However, it remains obscure how fungi respond to climate warming and whether fungi, in turn, affect carbon stability of tundra. In a 2-year winter soil warming experiment of 2°C by snow fences, we investigated responses of fungal communities to warming in the active layer of an Alaskan tundra. Although fungal community composition, revealed by the 28S rRNA gene amplicon sequencing, remained unchanged (p > .05), fungal functional gene composition, revealed by a microarray named GeoChip, was altered (p < .05). Changes in functional gene composition were linked to winter soil temperature, thaw depth, soil moisture, and gross primary productivity (canonical correlation analysis, p < .05). Specifically, relative abundances of fungal genes encoding invertase, xylose reductase and vanillin dehydrogenase significantly increased (p < .05), indicating higher carbon degradation capacities of fungal communities under warming. Accordingly, we detected changes in fungal gene networks under warming, including higher average path distance, lower average clustering coefficient and lower percentage of negative links, indicating that warming potentially changed fungal interactions. Together, our study revealsmore »
- Authors:
-
- Tsinghua University, Beijing (China)
- University of Oklahoma, Norman, OK (United States); University of California, Berkeley, CA (United States)
- University of Oklahoma, Norman, OK (United States)
- University of Oklahoma, Norman, OK (United States); University of California, San Francisco, CA (United States)
- Northern Arizona University, Flagstaff, AZ (United States)
- Michigan State University, East Lansing, MI (United States)
- Tsinghua University, Beijing (China); University of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation of China
- OSTI Identifier:
- 2318682
- Grant/Contract Number:
- SC0004601; SC0010715; AC02-05CH11231; 41877048; 41825016
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Ecology
- Additional Journal Information:
- Journal Volume: 30; Journal Issue: 4; Journal ID: ISSN 0962-1083
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Alaskan tundra; carbon degradation; functional gene; network analysis; soil fungal communities; winter warming
Citation Formats
Cheng, Jingmin, Yang, Yunfeng, Yuan, Mengting M., Gao, Qun, Wu, Liyou, Qin, Ziyan, Shi, Zhou J., Schuur, Edward G., Cole, James R., Tiedje, James M., and Zhou, Jizhong. Winter warming rapidly increases carbon degradation capacities of fungal communities in tundra soil: Potential consequences on carbon stability. United States: N. p., 2020.
Web. doi:10.1111/mec.15773.
Cheng, Jingmin, Yang, Yunfeng, Yuan, Mengting M., Gao, Qun, Wu, Liyou, Qin, Ziyan, Shi, Zhou J., Schuur, Edward G., Cole, James R., Tiedje, James M., & Zhou, Jizhong. Winter warming rapidly increases carbon degradation capacities of fungal communities in tundra soil: Potential consequences on carbon stability. United States. https://doi.org/10.1111/mec.15773
Cheng, Jingmin, Yang, Yunfeng, Yuan, Mengting M., Gao, Qun, Wu, Liyou, Qin, Ziyan, Shi, Zhou J., Schuur, Edward G., Cole, James R., Tiedje, James M., and Zhou, Jizhong. Thu .
"Winter warming rapidly increases carbon degradation capacities of fungal communities in tundra soil: Potential consequences on carbon stability". United States. https://doi.org/10.1111/mec.15773. https://www.osti.gov/servlets/purl/2318682.
@article{osti_2318682,
title = {Winter warming rapidly increases carbon degradation capacities of fungal communities in tundra soil: Potential consequences on carbon stability},
author = {Cheng, Jingmin and Yang, Yunfeng and Yuan, Mengting M. and Gao, Qun and Wu, Liyou and Qin, Ziyan and Shi, Zhou J. and Schuur, Edward G. and Cole, James R. and Tiedje, James M. and Zhou, Jizhong},
abstractNote = {We report high-latitude tundra ecosystems are increasingly affected by climate warming. As an important fraction of soil microorganisms, fungi play essential roles in carbon degradation, especially the old, chemically recalcitrant carbon. However, it remains obscure how fungi respond to climate warming and whether fungi, in turn, affect carbon stability of tundra. In a 2-year winter soil warming experiment of 2°C by snow fences, we investigated responses of fungal communities to warming in the active layer of an Alaskan tundra. Although fungal community composition, revealed by the 28S rRNA gene amplicon sequencing, remained unchanged (p > .05), fungal functional gene composition, revealed by a microarray named GeoChip, was altered (p < .05). Changes in functional gene composition were linked to winter soil temperature, thaw depth, soil moisture, and gross primary productivity (canonical correlation analysis, p < .05). Specifically, relative abundances of fungal genes encoding invertase, xylose reductase and vanillin dehydrogenase significantly increased (p < .05), indicating higher carbon degradation capacities of fungal communities under warming. Accordingly, we detected changes in fungal gene networks under warming, including higher average path distance, lower average clustering coefficient and lower percentage of negative links, indicating that warming potentially changed fungal interactions. Together, our study reveals higher carbon degradation capacities of fungal communities under short-term warming and highlights the potential impacts of fungal communities on tundra ecosystem respiration, and consequently future carbon stability of high-latitude tundra.},
doi = {10.1111/mec.15773},
journal = {Molecular Ecology},
number = 4,
volume = 30,
place = {United States},
year = {Thu Dec 10 00:00:00 EST 2020},
month = {Thu Dec 10 00:00:00 EST 2020}
}
Works referenced in this record:
Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition
journal, May 2007
- Blackwood, Christopher B.; Waldrop, Mark P.; Zak, Donald R.
- Environmental Microbiology, Vol. 9, Issue 5
Microbial interactions: from networks to models
journal, July 2012
- Faust, Karoline; Raes, Jeroen
- Nature Reviews Microbiology, Vol. 10, Issue 8
Microbial functional traits are sensitive indicators of mild disturbance by lamb grazing
journal, January 2019
- Ma, Xingyu; Zhang, Qiuting; Zheng, Mengmei
- The ISME Journal, Vol. 13, Issue 5
Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes
journal, April 2019
- Zhao, Mengxin; Sun, Bo; Wu, Linwei
- Molecular Ecology, Vol. 28, Issue 7
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
Influence of Growth Temperature on Lipid and Soluble Carbohydrate Synthesis by Fungi Isolated from Fellfield Soil in the Maritime Antarctic
journal, March 2000
- Weinstein, Richard N.; Montiel, Pedro O.; Johnstone, Keith
- Mycologia, Vol. 92, Issue 2
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
Utilization of ancient permafrost carbon in headwaters of Arctic fluvial networks
journal, July 2015
- Mann, Paul J.; Eglinton, Timothy I.; McIntyre, Cameron P.
- Nature Communications, Vol. 6, Issue 1
Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect
journal, May 2007
- Yergeau, Etienne; Kang, Sanghoon; He, Zhili
- The ISME Journal, Vol. 1, Issue 2
Mineralization and carbon turnover in subarctic heath soil as affected by warming and additional litter
journal, December 2007
- Rinnan, Riikka; Michelsen, Anders; Bååth, Erland
- Soil Biology and Biochemistry, Vol. 39, Issue 12
Long-term increase in snow depth leads to compositional changes in arctic ectomycorrhizal fungal communities
journal, June 2016
- Morgado, Luis N.; Semenova, Tatiana A.; Welker, Jeffrey M.
- Global Change Biology, Vol. 22, Issue 9
Decomposition of old organic matter as a result of deeper active layers in a snow depth manipulation experiment
journal, January 2010
- Nowinski, Nicole S.; Taneva, Lina; Trumbore, Susan E.
- Oecologia, Vol. 163, Issue 3
Drought-resistant fungi control soil organic matter decomposition and its response to temperature: FUNGAL DIVERSITY CONTROL OVER SOIL C BALANCE
journal, September 2010
- Yuste, J. C.; PeÑUelas, J.; Estiarte, M.
- Global Change Biology, Vol. 17, Issue 3
Heterotrophic soil respiration—Comparison of different models describing its temperature dependence
journal, February 2008
- Tuomi, Mikko; Vanhala, Pekka; Karhu, Kristiina
- Ecological Modelling, Vol. 211, Issue 1-2
Permafrost degradation stimulates carbon loss from experimentally warmed tundra
journal, March 2014
- Natali, Susan M.; Schuur, Edward A. G.; Webb, Elizabeth E.
- Ecology, Vol. 95, Issue 3
Labile and recalcitrant pools of carbon and nitrogen in organic matter decomposing at different depths in soil: an acid hydrolysis approach
journal, May 2002
- Rovira, Pere; Vallejo, V. Ramón
- Geoderma, Vol. 107, Issue 1-2
Seasonal Dynamics of Previously Unknown Fungal Lineages in Tundra Soils
journal, September 2003
- Schadt, C. W.
- Science, Vol. 301, Issue 5638
Bacterial and fungal community structure in Arctic tundra tussock and shrub soils: Community structure in Arctic tundra tussock and shrub soils
journal, February 2007
- Wallenstein, Matthew David; McMahon, Shawna; Schimel, Joshua
- FEMS Microbiology Ecology, Vol. 59, Issue 2
Keystone taxa as drivers of microbiome structure and functioning
journal, May 2018
- Banerjee, Samiran; Schlaeppi, Klaus; van der Heijden, Marcel G. A.
- Nature Reviews Microbiology, Vol. 16, Issue 9
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 seasonal pattern of soil microbial community structure in mesic low arctic tundra
journal, October 2013
- Buckeridge, Kate M.; Banerjee, Samiran; Siciliano, Steven D.
- Soil Biology and Biochemistry, Vol. 65
Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates
journal, September 2010
- de Graaff, Marie-Anne; Classen, Aimee T.; Castro, Hector F.
- New Phytologist, Vol. 188, Issue 4
Warming induced changes in soil carbon and nitrogen influence priming responses in four ecosystems
journal, March 2018
- Mau, Rebecca L.; Dijkstra, Paul; Schwartz, Egbert
- Applied Soil Ecology, Vol. 124
Enhanced summer warming reduces fungal decomposer diversity and litter mass loss more strongly in dry than in wet tundra
journal, June 2016
- Christiansen, Casper T.; Haugwitz, Merian S.; Priemé, Anders
- Global Change Biology, Vol. 23, Issue 1
Genetic Linkage of Soil Carbon Pools and Microbial Functions in Subtropical Freshwater Wetlands in Response to Experimental Warming
journal, August 2012
- Wang, Hang; He, Zhili; Lu, Zhenmei
- Applied and Environmental Microbiology, Vol. 78, Issue 21
Land use alters the resistance and resilience of soil food webs to drought
journal, January 2012
- de Vries, Franciska T.; Liiri, Mira E.; Bjørnlund, Lisa
- Nature Climate Change, Vol. 2, Issue 4
Climate sensitivity of shrub growth across the tundra biome
journal, July 2015
- Myers-Smith, Isla H.; Elmendorf, Sarah C.; Beck, Pieter S. A.
- Nature Climate Change, Vol. 5, Issue 9
Long-term warming alters the composition of Arctic soil microbial communities
journal, April 2012
- Deslippe, Julie R.; Hartmann, Martin; Simard, Suzanne W.
- FEMS Microbiology Ecology, Vol. 82, Issue 2
Responses of soil cellulolytic fungal communities to elevated atmospheric CO2 are complex and variable across five ecosystems: Response of cellulolytic fungi to elevated atmospheric CO2
journal, September 2011
- Weber, Carolyn F.; Zak, Donald R.; Hungate, Bruce A.
- Environmental Microbiology, Vol. 13, Issue 10
Microbial Community Composition and Function Across an Arctic Tundra Landscape
journal, July 2006
- Zak, Donald R.; Kling, George W.
- Ecology, Vol. 87, Issue 7
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
Pan-Arctic ice-wedge degradation in warming permafrost and its influence on tundra hydrology
journal, March 2016
- Liljedahl, Anna K.; Boike, Julia; Daanen, Ronald P.
- Nature Geoscience, Vol. 9, Issue 4
Warming enhances old organic carbon decomposition through altering functional microbial communities
journal, April 2017
- Cheng, Lei; Zhang, Naifang; Yuan, Mengting
- The ISME Journal, Vol. 11, Issue 8
Soil bacterial networks are less stable under drought than fungal networks
journal, August 2018
- de Vries, Franciska T.; Griffiths, Rob I.; Bailey, Mark
- Nature Communications, Vol. 9, Issue 1
Increasing shrub abundance in the Arctic
journal, May 2001
- Sturm, Matthew; Racine, Charles; Tape, Kenneth
- Nature, Vol. 411, Issue 6837
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
Long-term successional dynamics of microbial association networks in anaerobic digestion processes
journal, November 2016
- Wu, Linwei; Yang, Yunfeng; Chen, Si
- Water Research, Vol. 104
Warming-Induced Shrub Expansion and Lichen Decline in the Western Canadian Arctic
journal, July 2014
- Fraser, Robert H.; Lantz, Trevor C.; Olthof, Ian
- Ecosystems, Vol. 17, Issue 7
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
journal, March 2015
- Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
- Nature, Vol. 521, Issue 7551
Ectomycorrhizal and saprotrophic fungi respond differently to long‐term experimentally increased snow depth in the High Arctic
journal, June 2016
- Mundra, Sunil; Halvorsen, Rune; Kauserud, Håvard
- MicrobiologyOpen, Vol. 5, Issue 5
Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance
journal, January 2020
- Wu, Linwei; Shan, Xiaoyu; Chen, Si
- mSystems, Vol. 5, Issue 1
Global diversity and geography of soil fungi
journal, November 2014
- Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei
- Science, Vol. 346, Issue 6213
Analyses of ITS and LSU gene regions provide congruent results on fungal community responses
journal, June 2014
- Brown, Shawn P.; Rigdon-Huss, Anne R.; Jumpponen, Ari
- Fungal Ecology, Vol. 9
Physiological and molecular aspects of degradation of plant polysaccharides by fungi: What have we learned from Aspergillus ?
journal, May 2013
- Culleton, Helena; McKie, Vincent; de Vries, Ronald P.
- Biotechnology Journal, Vol. 8, Issue 8
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
Permafrost Destabilization and Thermokarst Following Snow Fence Installation, Barrow, Alaska, U.S.A
journal, November 2006
- Hinkel, Kenneth M.; Hurd, John K.
- Arctic, Antarctic, and Alpine Research, Vol. 38, Issue 4
Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems
journal, August 2014
- Levy-Booth, David J.; Prescott, Cindy E.; Grayston, Susan J.
- Soil Biology and Biochemistry, Vol. 75
Mineral fertilizer alters cellulolytic community structure and suppresses soil cellobiohydrolase activity in a long-term fertilization experiment
journal, December 2012
- Fan, Fenliang; Li, Zhaojun; Wakelin, Steven A.
- Soil Biology and Biochemistry, Vol. 55
Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost: Increased plant productivity in Alaskan tundra
journal, November 2011
- Natali, Susan M.; Schuur, Edward A. G.; Rubin, Rachel L.
- Journal of Ecology, Vol. 100, Issue 2
Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil
journal, June 2016
- Banerjee, Samiran; Kirkby, Clive A.; Schmutter, Dione
- Soil Biology and Biochemistry, Vol. 97
Microbial community structure and its functional implications
journal, May 2009
- Fuhrman, Jed A.
- Nature, Vol. 459, Issue 7244
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016
- Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
- Ecology Letters, Vol. 19, Issue 8
Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems
journal, July 2006
- Clemmensen, Karina E.; Michelsen, Anders; Jonasson, Sven
- New Phytologist, Vol. 171, Issue 2
Rich and cold: diversity, distribution and drivers of fungal communities in patterned-ground ecosystems of the North American Arctic
journal, April 2014
- Timling, I.; Walker, D. A.; Nusbaum, C.
- Molecular Ecology, Vol. 23, Issue 13
Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi
journal, May 2008
- Malcolm, Glenna M.; LÓPez-GutiÉRrez, Juan C.; Koide, Roger T.
- Global Change Biology, Vol. 14, Issue 5
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
Functional cartography of complex metabolic networks
journal, February 2005
- Guimerà, Roger; Nunes Amaral, Luís A.
- Nature, Vol. 433, Issue 7028
Compositional and functional shifts in arctic fungal communities in response to experimentally increased snow depth
journal, September 2016
- Semenova, Tatiana A.; Morgado, Luis N.; Welker, Jeffrey M.
- Soil Biology and Biochemistry, Vol. 100