skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil

Abstract

Nitrogen (N) deposition is a component of global change that has considerable impact on belowground carbon (C) dynamics. Plant growth stimulation and alterations of fungal community composition and functions are the main mechanisms driving soil C gains following N deposition in N-limited temperate forests. In N-rich tropical forests, however, N deposition generally has minor effects on plant growth; consequently, C storage in soil may strongly depend on the microbial processes that drive litter and soil organic matter decomposition. Here, we investigated how microbial functions in old-growth tropical forest soil responded to 13 years of N addition at four rates: 0 (Control), 50 (Low-N), 100 (Medium-N), and 150 (High-N) kg N ha-1 year-1. Soil organic carbon (SOC) content increased under High-N, corresponding to a 33% decrease in CO2 efflux, and reductions in relative abundances of bacteria as well as genes responsible for cellulose and chitin degradation. A 113% increase in N2O emission was positively correlated with soil acidification and an increase in the relative abundances of denitrification genes (narG and norB). Soil acidification induced by N addition decreased available P concentrations, and was associated with reductions in the relative abundance of phytase. The decreased relative abundance of bacteria and key functional gene groups formore » C degradation were related to slower SOC decomposition, indicating the key mechanisms driving SOC accumulation in the tropical forest soil subjected to High-N addition. However, changes in microbial functional groups associated with N and P cycling led to coincidentally large increases in N2O emissions, and exacerbated soil P deficiency. These two factors partially offset the perceived beneficial effects of N addition on SOC storage in tropical forest soils. Finally, these findings suggest a potential to incorporate microbial community and functions into Earth system models considering their effects on greenhouse gas emission, biogeochemical processes, and biodiversity of tropical ecosystems.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [4];  [2];  [3]; ORCiD logo [3]; ORCiD logo [5];  [6]; ORCiD logo [7]
  1. China Agricultural Univ., Beijing (China); Chinese Academy of Sciences (CAS), Beijing (China). Key Lab. of Ecosystem Network Observation and Modeling, Inst. of Geographic Sciences and Natural Resources Research
  2. Univ. of Exeter, Exeter (United Kingdom)
  3. Chinese Academy of Sciences (CAS), Guangzhou (China). Key Lab. of Vegetation Restoration and Management of Degraded Ecosystems and Guangdong Provincial Key Lab. of Applied Botany
  4. Tsinghua Univ., Beijing (China)
  5. Chinese Academy of Sciences (CAS), Beijing (China). Key Lab. of Ecosystem Network Observation and Modeling, Inst. of Geographic Sciences and Natural Resources Research
  6. Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of Gottingen, Gottingen (Germany); Central South Univ. of Forestry and Technology, Changsha (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Natural Science Foundation of China (NNSFC); National Key R&D Program of China
OSTI Identifier:
1580939
Grant/Contract Number:  
AC02-05CH11231; 31770560; 41571130041; 41731176; 2017YFA0604803; LENOM2016Q0004
Resource Type:
Accepted Manuscript
Journal Name:
Global Change Biology
Additional Journal Information:
Journal Volume: 25; Journal Issue: 10; Journal ID: ISSN 1354-1013
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biogeochemical cycling; C and N turnover; global climate change; microbial functional community; N deposition; tropical forest

Citation Formats

Tian, Jing, Dungait, Jennifer A. J., Lu, Xiankai, Yang, Yunfeng, Hartley, Iain P., Zhang, Wei, Mo, Jiangming, Yu, Guirui, Zhou, Jizhong, and Kuzyakov, Yakov. Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil. United States: N. p., 2019. Web. doi:10.1111/gcb.14750.
Tian, Jing, Dungait, Jennifer A. J., Lu, Xiankai, Yang, Yunfeng, Hartley, Iain P., Zhang, Wei, Mo, Jiangming, Yu, Guirui, Zhou, Jizhong, & Kuzyakov, Yakov. Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil. United States. doi:https://doi.org/10.1111/gcb.14750
Tian, Jing, Dungait, Jennifer A. J., Lu, Xiankai, Yang, Yunfeng, Hartley, Iain P., Zhang, Wei, Mo, Jiangming, Yu, Guirui, Zhou, Jizhong, and Kuzyakov, Yakov. Fri . "Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil". United States. doi:https://doi.org/10.1111/gcb.14750. https://www.osti.gov/servlets/purl/1580939.
@article{osti_1580939,
title = {Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil},
author = {Tian, Jing and Dungait, Jennifer A. J. and Lu, Xiankai and Yang, Yunfeng and Hartley, Iain P. and Zhang, Wei and Mo, Jiangming and Yu, Guirui and Zhou, Jizhong and Kuzyakov, Yakov},
abstractNote = {Nitrogen (N) deposition is a component of global change that has considerable impact on belowground carbon (C) dynamics. Plant growth stimulation and alterations of fungal community composition and functions are the main mechanisms driving soil C gains following N deposition in N-limited temperate forests. In N-rich tropical forests, however, N deposition generally has minor effects on plant growth; consequently, C storage in soil may strongly depend on the microbial processes that drive litter and soil organic matter decomposition. Here, we investigated how microbial functions in old-growth tropical forest soil responded to 13 years of N addition at four rates: 0 (Control), 50 (Low-N), 100 (Medium-N), and 150 (High-N) kg N ha-1 year-1. Soil organic carbon (SOC) content increased under High-N, corresponding to a 33% decrease in CO2 efflux, and reductions in relative abundances of bacteria as well as genes responsible for cellulose and chitin degradation. A 113% increase in N2O emission was positively correlated with soil acidification and an increase in the relative abundances of denitrification genes (narG and norB). Soil acidification induced by N addition decreased available P concentrations, and was associated with reductions in the relative abundance of phytase. The decreased relative abundance of bacteria and key functional gene groups for C degradation were related to slower SOC decomposition, indicating the key mechanisms driving SOC accumulation in the tropical forest soil subjected to High-N addition. However, changes in microbial functional groups associated with N and P cycling led to coincidentally large increases in N2O emissions, and exacerbated soil P deficiency. These two factors partially offset the perceived beneficial effects of N addition on SOC storage in tropical forest soils. Finally, these findings suggest a potential to incorporate microbial community and functions into Earth system models considering their effects on greenhouse gas emission, biogeochemical processes, and biodiversity of tropical ecosystems.},
doi = {10.1111/gcb.14750},
journal = {Global Change Biology},
number = 10,
volume = 25,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem
journal, January 2016


Denitrification and total nitrogen gas production from forest soils of Eastern China
journal, December 2009


Net greenhouse gas balance in response to nitrogen enrichment: perspectives from a coupled biogeochemical model
journal, November 2012

  • Lu, Chaoqun; Tian, Hanqin
  • Global Change Biology, Vol. 19, Issue 2
  • DOI: 10.1111/gcb.12049

Divergent Responses of Soil Buffering Capacity to Long-Term N Deposition in Three Typical Tropical Forests with Different Land-Use History
journal, March 2015

  • Lu, Xiankai; Mao, Qinggong; Mo, Jiangming
  • Environmental Science & Technology, Vol. 49, Issue 7
  • DOI: 10.1021/es5047233

Nitrogen fertilization raises CO 2 efflux from inorganic carbon: A global assessment
journal, April 2018

  • Zamanian, Kazem; Zarebanadkouki, Mohsen; Kuzyakov, Yakov
  • Global Change Biology, Vol. 24, Issue 7
  • DOI: 10.1111/gcb.14148

Nutrient limitation of soil microbial processes in tropical forests
journal, November 2017

  • Camenzind, Tessa; Hättenschwiler, Stephan; Treseder, Kathleen K.
  • Ecological Monographs, Vol. 88, Issue 1
  • DOI: 10.1002/ecm.1279

Short and long-term impacts of nitrogen deposition on carbon sequestration by forest ecosystems
journal, November 2014

  • de Vries, Wim; Du, Enzai; Butterbach-Bahl, Klaus
  • Current Opinion in Environmental Sustainability, Vol. 9-10
  • DOI: 10.1016/j.cosust.2014.09.001

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

Increased fungal dominance in N2O emission hotspots along a natural pH gradient in organic forest soil
journal, December 2012


Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies
journal, October 2008


Microbial adaptation to long-term N supply prevents large responses in N dynamics and N losses of a subtropical forest
journal, June 2018


The mechanisms governing low denitrification capacity and high nitrogen oxide gas emissions in subtropical forest soils in China: Denitrification in subtropical soil
journal, August 2014

  • Zhang, Jinbo; Yu, Yongjie; Zhu, Tongbin
  • Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 8
  • DOI: 10.1002/2014JG002662

Combined effects of nitrogen addition and organic matter manipulation on soil respiration in a Chinese pine forest
journal, August 2016

  • Wang, Jinsong; Wu, L.; Zhang, Chunyu
  • Environmental Science and Pollution Research, Vol. 23, Issue 22
  • DOI: 10.1007/s11356-016-7474-7

Rice, microbes and methane
journal, January 2000


Specific microbial gene abundances and soil parameters contribute to C, N, and greenhouse gas process rates after land use change in Southern Amazonian Soils
journal, October 2015

  • Lammel, Daniel R.; Feigl, Brigitte J.; Cerri, Carlos C.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01057

Effects of nitrogen deposition on the greenhouse gas fluxes from forest soils
journal, May 2008


Global methane and nitrous oxide emissions from terrestrial ecosystems due to multiple environmental changes
journal, March 2015

  • Tian, Hanqin; Chen, Guangsheng; Lu, Chaoqun
  • Ecosystem Health and Sustainability, Vol. 1, Issue 1
  • DOI: 10.1890/EHS14-0015.1

Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest
journal, March 2013


Responses of Methanogen mcrA Genes and Their Transcripts to an Alternate Dry/Wet Cycle of Paddy Field Soil
journal, November 2011

  • Ma, Ke; Conrad, Ralf; Lu, Yahai
  • Applied and Environmental Microbiology, Vol. 78, Issue 2
  • DOI: 10.1128/AEM.06934-11

Global negative effects of nitrogen deposition on soil microbes
journal, March 2018


Nitrogen addition reduces soil respiration in a mature tropical forest in southern China: NITROGEN ADDITION SOUTHERN CHINA
journal, November 2007


Nitrogen transformations in a range of tropical forest soils
journal, January 1988


Global change effects on humid tropical forests: Evidence for biogeochemical and biodiversity shifts at an ecosystem scale: Tropical Forests and Global Change
journal, August 2016

  • Cusack, Daniela F.; Karpman, Jason; Ashdown, Daniel
  • Reviews of Geophysics, Vol. 54, Issue 3
  • DOI: 10.1002/2015RG000510

Scale-dependent key drivers controlling methane oxidation potential in Chinese grassland soils
journal, August 2017


Enhanced nitrogen deposition over China
journal, February 2013


Changes in CH4 production during different stages of litter decomposition under inundation and N addition
journal, December 2016


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


Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis
journal, January 2016

  • Li, Yong; Niu, Shuli; Yu, Guirui
  • Global Change Biology, Vol. 22, Issue 2
  • DOI: 10.1111/gcb.13125

Plant acclimation to long-term high nitrogen deposition in an N-rich tropical forest
journal, May 2018

  • Lu, Xiankai; Vitousek, Peter M.; Mao, Qinggong
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 20
  • DOI: 10.1073/pnas.1720777115

A Coherent Signature of Anthropogenic Nitrogen Deposition to Remote Watersheds of the Northern Hemisphere
journal, December 2011


Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions
journal, January 2010

  • Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z.
  • Ecological Applications, Vol. 20, Issue 1
  • DOI: 10.1890/08-0127.1

Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition
journal, October 2016

  • Zak, Donald R.; Freedman, Zachary B.; Upchurch, Rima A.
  • Global Change Biology, Vol. 23, Issue 2
  • DOI: 10.1111/gcb.13480

The globalization of N deposition: ecosystem consequences in tropical environments
journal, July 1999

  • Matson, Pamela A.; McDowell, William H.; Townsend, Alan R.
  • Biogeochemistry, Vol. 46, Issue 1-3
  • DOI: 10.1007/BF01007574

The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil
journal, April 1996

  • Frosteg�rd, A.; B��th, E.
  • Biology and Fertility of Soils, Vol. 22, Issue 1-2
  • DOI: 10.1007/BF00384433

Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama
journal, June 2010

  • Corre, Marife D.; Veldkamp, Edzo; Arnold, Julia
  • Ecology, Vol. 91, Issue 6
  • DOI: 10.1890/09-0274.1

Meta-analyses of the effects of major global change drivers on soil respiration across China
journal, February 2017


Nitrogen Cycles: Past, Present, and Future
journal, September 2004


Microbial biomass measured as total lipid phosphate in soils of different organic content
journal, December 1991


Spatial and temporal variability of soil nitric oxide emissions in N-saturated subtropical forest
journal, August 2017


Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China
journal, October 2014


Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition
journal, May 2018


Are there links between responses of soil microbes and ecosystem functioning to elevated CO 2 , N deposition and warming? A global perspective
journal, December 2014

  • García-Palacios, Pablo; Vandegehuchte, Martijn L.; Shaw, E. Ashley
  • Global Change Biology, Vol. 21, Issue 4
  • DOI: 10.1111/gcb.12788

Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests
journal, April 2015

  • Hesse, Cedar N.; Mueller, Rebecca C.; Vuyisich, Momchilo
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00337

The Asian Nitrogen Cycle Case Study
journal, March 2002

  • Zheng, Xunhua; Fu, Congbin; Xu, Xingkai
  • AMBIO: A Journal of the Human Environment, Vol. 31, Issue 2
  • DOI: 10.1579/0044-7447-31.2.79

Rhizosphere priming effects on soil carbon and nitrogen mineralization
journal, September 2014


Soil organic matter turnover is governed by accessibility not recalcitrance
journal, March 2012


Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland
journal, November 2012

  • Yang, Yunfeng; Wu, Linwei; Lin, Qiaoyan
  • Global Change Biology, Vol. 19, Issue 2
  • DOI: 10.1111/gcb.12065

Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest
journal, June 2017

  • Kaspari, Michael; Bujan, Jelena; Weiser, Michael D.
  • Ecology, Vol. 98, Issue 8
  • DOI: 10.1002/ecy.1895

The Nitrogen Paradox in Tropical Forest Ecosystems
journal, December 2009


Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three?
journal, October 2006


Temporal changes in diversity and expression patterns of fungal laccase genes within the organic horizon of a brown forest soil
journal, July 2009


Carbon and macronutrient losses during accelerated erosion under different tillage and residue management: Soil C, N and P losses during erosion
journal, December 2014

  • Beniston, J. W.; Shipitalo, M. J.; Lal, R.
  • European Journal of Soil Science, Vol. 66, Issue 1
  • DOI: 10.1111/ejss.12205

Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization
journal, February 2018

  • Carrara, Joseph E.; Walter, Christopher A.; Hawkins, Jennifer S.
  • Global Change Biology, Vol. 24, Issue 6
  • DOI: 10.1111/gcb.14081

Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests
journal, July 2004


Patterns and mechanisms of responses by soil microbial communities to nitrogen addition
journal, December 2017


Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests
journal, March 2011

  • Cusack, Daniela F.; Silver, Whendee L.; Torn, Margaret S.
  • Ecology, Vol. 92, Issue 3
  • DOI: 10.1890/10-0459.1

Sources of CO2 efflux from soil and review of partitioning methods
journal, March 2006


Biological Nitrogen Fixation in Two Tropical Forests: Ecosystem-Level Patterns and Effects of Nitrogen Fertilization
journal, October 2009


Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem
journal, February 2007

  • Ramette, A.; Tiedje, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 8
  • DOI: 10.1073/pnas.0610671104

Old-Growth Forests Can Accumulate Carbon in Soils
journal, December 2006


Nitrogen deposition affects both net and gross soil nitrogen transformations in forest ecosystems: A review
journal, January 2019


Detecting active methanogenic populations on rice roots using stable isotope probing
journal, March 2005


Ecology of Nitrogen Fixing, Nitrifying, and Denitrifying Microorganisms in Tropical Forest Soils
journal, July 2016


Effect of land use on the denitrification, abundance of denitrifiers, and total nitrogen gas production in the subtropical region of China
journal, July 2013


Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization
journal, January 2009

  • Rousk, J.; Brookes, P. C.; Baath, E.
  • Applied and Environmental Microbiology, Vol. 75, Issue 6
  • DOI: 10.1128/AEM.02775-08

Effects of elevated nitrogen deposition on soil microbial biomass carbon in major subtropical forests of southern China
journal, January 2009


Reduction of forest soil respiration in response to nitrogen deposition
journal, April 2010

  • Janssens, I. A.; Dieleman, W.; Luyssaert, S.
  • Nature Geoscience, Vol. 3, Issue 5
  • DOI: 10.1038/ngeo844

Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems
journal, August 2014


Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA
journal, July 2004


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
  • DOI: 10.1038/ismej.2010.8

Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation
journal, November 2012


Soil carbon release enhanced by increased tropical forest litterfall
journal, August 2011

  • Sayer, Emma J.; Heard, Matthew S.; Grant, Helen K.
  • Nature Climate Change, Vol. 1, Issue 6
  • DOI: 10.1038/nclimate1190

Plant-mediated CH 4 transport and contribution of photosynthates to methanogenesis at a boreal mire: a 14 C pulse-labeling study
journal, January 2011


Nitrogen deposition promotes ecosystem carbon accumulation by reducing soil carbon emission in a subtropical forest
journal, March 2014


Tropical forests are a net carbon source based on aboveground measurements of gain and loss
journal, September 2017


Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition
journal, April 2013

  • Eisenlord, Sarah D.; Freedman, Zachary; Zak, Donald R.
  • Applied and Environmental Microbiology, Vol. 79, Issue 8
  • DOI: 10.1128/AEM.00468-13

Review: Factors affecting rhizosphere priming effects
journal, August 2002


Resource availability controls fungal diversity across a plant diversity gradient: Resource availability controls fungal diversity
journal, September 2006


Cumulative effects of nitrogen additions on litter decomposition in three tropical forests in southern China
journal, July 2007


    Works referencing / citing this record:

    Soil GHG fluxes are altered by N deposition: New data indicate lower N stimulation of the N 2 O flux and greater stimulation of the calculated C pools
    journal, January 2020

    • Deng, Lei; Huang, Chunbo; Kim, Dong‐Gill
    • Global Change Biology, Vol. 26, Issue 4
    • DOI: 10.1111/gcb.14970