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

Journal Article · · Global Change Biology
DOI: https://doi.org/10.1111/gcb.14750 · OSTI ID:1580939
 [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)

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
National Key R&D Program of China; National Natural Science Foundation of China (NNSFC); USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1580939
Journal Information:
Global Change Biology, Journal Name: Global Change Biology Journal Issue: 10 Vol. 25; ISSN 1354-1013
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (102)

Review: Factors affecting rhizosphere priming effects journal August 2002
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
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
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
Nutrient limitation of soil microbial processes in tropical forests journal November 2017
Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest journal June 2017
The globalization of N deposition: ecosystem consequences in tropical environments book January 1999
The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil journal April 1996
The globalization of N deposition: ecosystem consequences in tropical environments journal July 1999
Are Basidiomycete Laccase Gene Abundance and Composition Related to Reduced Lignolytic Activity Under Elevated Atmospheric NO3 − Deposition in a Northern Hardwood Forest? journal September 2008
Impacts of Carbon and Flooding on Soil Microbial Communities: Phospholipid Fatty Acid Profiles and Substrate Utilization Patterns journal May 1998
Increased fungal dominance in N2O emission hotspots along a natural pH gradient in organic forest soil journal December 2012
Effect of land use on the denitrification, abundance of denitrifiers, and total nitrogen gas production in the subtropical region of China journal July 2013
Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China journal October 2014
The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil journal April 1996
Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? journal October 2006
Biological Nitrogen Fixation in Two Tropical Forests: Ecosystem-Level Patterns and Effects of Nitrogen Fertilization journal October 2009
Nitrogen Cycles: Past, Present, and Future journal September 2004
Spatial and temporal variability of soil nitric oxide emissions in N-saturated subtropical forest journal August 2017
Cumulative effects of nitrogen additions on litter decomposition in three tropical forests in southern China journal July 2007
Cumulative effects of nitrogen additions on litter decomposition in three tropical forests in southern China journal February 2009
Nitrogen deposition promotes ecosystem carbon accumulation by reducing soil carbon emission in a subtropical forest journal March 2014
Combined effects of nitrogen addition and organic matter manipulation on soil respiration in a Chinese pine forest journal August 2016
Photosynthesis acclimation, leaf nitrogen concentration, and growth of four tree species over 3 years in response to elevated carbon dioxide and nitrogen treatment in subtropical China journal July 2011
Changes in CH4 production during different stages of litter decomposition under inundation and N addition journal December 2016
Effects of elevated nitrogen deposition on soil microbial biomass carbon in major subtropical forests of southern China journal January 2009
Nitrogen transformations in a range of tropical forest soils journal January 1988
Microbial biomass measured as total lipid phosphate in soils of different organic content journal December 1991
Effects of nitrogen deposition on the greenhouse gas fluxes from forest soils journal May 2008
Meta-analyses of the effects of major global change drivers on soil respiration across China journal February 2017
Short and long-term impacts of nitrogen deposition on carbon sequestration by forest ecosystems journal November 2014
Nitrogen deposition affects both net and gross soil nitrogen transformations in forest ecosystems: A review journal January 2019
Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests journal July 2004
Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA journal July 2004
Microbial adaptation to long-term N supply prevents large responses in N dynamics and N losses of a subtropical forest journal June 2018
Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil journal May 2006
Sources of CO2 efflux from soil and review of partitioning methods journal March 2006
Temporal changes in diversity and expression patterns of fungal laccase genes within the organic horizon of a brown forest soil journal July 2009
Denitrification and total nitrogen gas production from forest soils of Eastern China journal December 2009
Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems journal August 2014
Rhizosphere priming effects on soil carbon and nitrogen mineralization journal September 2014
Parent material and vegetation influence bacterial community structure and nitrogen functional genes along deep tropical soil profiles at the Luquillo Critical Zone Observatory journal January 2015
Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem journal January 2016
Scale-dependent key drivers controlling methane oxidation potential in Chinese grassland soils journal August 2017
Patterns and mechanisms of responses by soil microbial communities to nitrogen addition journal December 2017
Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition journal May 2018
Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation journal November 2012
Divergent Responses of Soil Buffering Capacity to Long-Term N Deposition in Three Typical Tropical Forests with Different Land-Use History journal March 2015
Methane uptake responses to nitrogen deposition in three tropical forests in southern China journal June 2008
Rice, microbes and methane journal January 2000
GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity journal April 2010
Bacterial gene abundances as indicators of greenhouse gas emission in soils journal February 2010
Enhanced nitrogen deposition over China journal February 2013
Soil carbon release enhanced by increased tropical forest litterfall journal August 2011
Microbial mediation of carbon-cycle feedbacks to climate warming journal December 2011
Microbial diversity drives multifunctionality in terrestrial ecosystems journal January 2016
Reduction of forest soil respiration in response to nitrogen deposition journal April 2010
Global negative effects of nitrogen deposition on soil microbes journal March 2018
Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem journal February 2007
Plant acclimation to long-term high nitrogen deposition in an N-rich tropical forest journal May 2018
Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils: Urea-linked archaeal ammonia oxidation in acid soil journal January 2013
Carbon and macronutrient losses during accelerated erosion under different tillage and residue management: Soil C, N and P losses during erosion journal December 2014
Net greenhouse gas balance in response to nitrogen enrichment: perspectives from a coupled biogeochemical model journal November 2012
Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland journal November 2012
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
Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis journal January 2016
Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition journal October 2016
Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization journal February 2018
Nitrogen fertilization raises CO 2 efflux from inorganic carbon: A global assessment journal April 2018
Nitrogen addition reduces soil respiration in a mature tropical forest in southern China: NITROGEN ADDITION SOUTHERN CHINA journal November 2007
Soil organic matter turnover is governed by accessibility not recalcitrance journal March 2012
Resource availability controls fungal diversity across a plant diversity gradient: Resource availability controls fungal diversity journal September 2006
Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies journal October 2008
A review of nitrogen enrichment effects on three biogenic GHGs: the CO 2 sink may be largely offset by stimulated N 2 O and CH 4 emission journal October 2009
Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis: Nutrients, climate and tropical NPP journal July 2011
Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis: Errata journal November 2011
Detecting active methanogenic populations on rice roots using stable isotope probing journal March 2005
Denitrification gene pools, transcription and kinetics of  NO, N2O and N2 production as affected by soil pH: Gene transcription, gas kinetics as affected by soil pH journal February 2010
A keystone microbial enzyme for nitrogen control of soil carbon storage journal August 2018
Old-Growth Forests Can Accumulate Carbon in Soils journal December 2006
A Coherent Signature of Anthropogenic Nitrogen Deposition to Remote Watersheds of the Northern Hemisphere journal December 2011
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest journal March 2013
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
Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization journal January 2009
Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition journal December 2012
Responses of Methanogen mcrA Genes and Their Transcripts to an Alternate Dry/Wet Cycle of Paddy Field Soil journal November 2011
Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition journal April 2013
Responses of Methanogen mcrA Genes and Their Transcripts to an Alternate Dry/Wet Cycle of Paddy Field Soil journal November 2011
The Nitrogen Paradox in Tropical Forest Ecosystems journal December 2009
The Asian Nitrogen Cycle Case Study journal March 2002
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions journal January 2010
Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama journal June 2010
Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests journal March 2011
Global methane and nitrous oxide emissions from terrestrial ecosystems due to multiple environmental changes journal March 2015
Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests journal April 2015
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
Ecology of Nitrogen Fixing, Nitrifying, and Denitrifying Microorganisms in Tropical Forest Soils journal July 2016
Plant-mediated CH 4 transport and contribution of photosynthates to methanogenesis at a boreal mire: a 14 C pulse-labeling study journal January 2011
Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama collection January 2016
Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests collection January 2016
Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem text January 2007

Cited By (1)