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Title: Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling

Journal Article · · Global Change Biology
DOI:https://doi.org/10.1111/gcb.14962· OSTI ID:1595151
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [4]; ORCiD logo [3]; ORCiD logo [5]
  1. Lawrence Berkeley National Laboratory Climate and Ecosystem Science Division Berkeley CA USA
  2. Department of Biology University of Antwerp Wilrijk Belgium, Centre for Microbiology and Environmental Systems Science University of Vienna Vienna Austria
  3. Center for Ecological Research and Forestry Application Bellaterra Catalonia Spain, Global Ecology Unit CREAF‐CSIC‐UAB Bellaterra Catalonia Spain
  4. Department of Biology University of Antwerp Wilrijk Belgium
  5. Centre for Microbiology and Environmental Systems Science University of Vienna Vienna Austria, Ecosystems Services and Management Program International Institute for Applied Systems Analysis Laxenburg Austria

Abstract Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant‐centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be ‘limited’ by nutrients or carbon alone. Here, we outline how models aimed at predicting non‐steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant–microbe interactions in coupled carbon and nutrient models.

Sponsoring Organization:
USDOE
Grant/Contract Number:
DE‐AD01‐05CH11231
OSTI ID:
1595151
Journal Information:
Global Change Biology, Journal Name: Global Change Biology Vol. 26 Journal Issue: 4; ISSN 1354-1013
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 191 works
Citation information provided by
Web of Science

References (90)

Nutrient Limitation on Ecosystem Productivity and Processes of Mature and Old-Growth Subtropical Forests in China journal December 2012
Nutrients limiting microbial growth in a tropical forest soil of Ghana under different management journal May 1998
Representing life in the Earth system with soil microbial functional traits in the MIMICS model journal January 2015
Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake journal June 1996
Nutrient limitation of soil microbial processes in tropical forests journal November 2017
Clarifying the interpretation of carbon use efficiency in soil through methods comparison journal January 2019
The whole-soil carbon flux in response to warming journal March 2017
Multiple resource limitation theory applied to herbivorous consumers: Liebig’s minimum rule vs. interactive co-limitation: Co-limitation theory applied to herbivores journal December 2011
Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland journal June 2016
Is available carbon limiting microbial respiration in the rhizosphere? journal October 1996
Pervasive phosphorus limitation of tree species but not communities in tropical forests journal March 2018
Atmosphere–soil carbon transfer as a function of soil depth journal July 2018
Variable effects of nitrogen additions on the stability and turnover of soil carbon journal October 2002
Equivalence of microbial biomass measures based on membrane lipid and cell wall components, adenosine triphosphate, and direct counts in subsurface aquifer sediments journal July 1988
Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest journal September 2014
Enzyme properties down the soil profile - A matter of substrate quality in rhizosphere and detritusphere journal December 2016
Environmental and stoichiometric controls on microbial carbon-use efficiency in soils: Research review journal July 2012
Active microorganisms in soil: Critical review of estimation criteria and approaches journal December 2013
Elevated moisture stimulates carbon loss from mineral soils by releasing protected organic matter journal November 2017
Evaluating litter decomposition in earth system models with long-term litterbag experiments: an example using the Community Land Model version 4 (CLM4) journal October 2012
ORCHIMIC (v1.0), a microbe-mediated model for soil organic matter decomposition journal January 2018
Interactions between Carbon and Nitrogen Mineralization and Soil Organic Matter Chemistry in Arctic Tundra Soils journal March 2003
Phosphorus mineralization can be driven by microbial need for carbon journal June 2013
Nutrient limitation and soil development: Experimental test of a biogeochemical theory journal April 1997
Carbon and Nitrogen Amendments Lead to Differential Growth of Bacterial and Fungal Communities in a High-pH Soil journal April 2018
Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization journal September 2004
Microbial nitrogen dynamics in organic and mineral soil horizons along a latitudinal transect in western Siberia: N DYNAMICS ALONG A LATITUDINAL TRANSECT journal May 2015
Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories journal April 2014
A representation of the phosphorus cycle for ORCHIDEE (revision 4520) journal January 2017
Long-term warming restructures Arctic tundra without changing net soil carbon storage journal May 2013
Review of mechanisms and quantification of priming effects journal October 2000
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions journal January 2010
Embracing the unknown: disentangling the complexities of the soil microbiome journal August 2017
Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil–litter interface journal July 2003
Field-experiment constraints on the enhancement of the terrestrial carbon sink by CO2 fertilization journal September 2019
Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources journal January 2014
Microbial hotspots and hot moments in soil: Concept & review journal April 2015
Quantitative Microbial Ecology through Stable Isotope Probing journal August 2015
Biomass production efficiency controlled by management in temperate and boreal ecosystems journal October 2015
Differential priming of soil carbon driven by soil depth and root impacts on carbon availability journal February 2014
The C:N:P stoichiometry of organisms and ecosystems in a changing world: A review and perspectives journal February 2012
Addition of inorganic phosphorus to soil leads to desorption of organic compounds and thus to increased soil respiration journal March 2019
The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest journal April 2013
Rhizosphere priming effects on soil carbon and nitrogen mineralization journal September 2014
Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response journal October 2009
Nitrogen and phosphorus constrain labile and stable carbon turnover in lowland tropical forest soils journal January 2015
A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems: Global soil microbial biomass C, N and P journal December 2012
Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability journal January 2008
Microbial dormancy improves development and experimental validation of ecosystem model journal July 2014
GOLUM-CNP v1.0: a data-driven modeling of carbon, nitrogen and phosphorus cycles in major terrestrial biomes journal January 2018
Optima and Limiting Factors journal April 1905
Amazon forest response to CO2 fertilization dependent on plant phosphorus acquisition journal August 2019
Nitrogen Availability and Nitrogen Use Efficiency in Loblolly Pine Stands journal February 1986
Increased water-use efficiency and reduced CO2 uptake by plants during droughts at a continental scale journal August 2018
An extraction method for measuring soil microbial biomass C journal January 1987
A plant–microbe interaction framework explaining nutrient effects on primary production journal September 2018
Plant Allocation and the Multiple Limitation Hypothesis journal June 1992
The application of ecological stoichiometry to plant–microbial–soil organic matter transformations journal May 2015
The contentious nature of soil organic matter journal November 2015
Root litter decomposition slows with soil depth journal October 2018
Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe journal December 2013
Microbial carbon use efficiency and biomass turnover times depending on soil depth – Implications for carbon cycling journal May 2016
Coupled carbon and nitrogen losses in response to seven years of chronic warming in subarctic soils journal July 2019
The Effect of the Addition of Organic Materials on the Decomposition of an Organic Soil1 journal January 1953
Formation of soil organic matter via biochemical and physical pathways of litter mass loss journal September 2015
Carbon and nitrogen dynamics along the decay continuum: Plant litter to soil organic matter journal April 1989
Nutrient amendment does not increase mineralisation of sequestered carbon during incubation of a nitrogen limited mangrove soil journal February 2013
Fertile forests produce biomass more efficiently: Forests’ biomass production efficiency journal April 2012
C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? journal July 2007
Are microorganisms more effective than plants at competing for nitrogen? journal July 2000
Priming of soil organic matter decomposition scales linearly with microbial biomass response to litter input in steppe vegetation journal November 2014
Growth of saprotrophic fungi and bacteria in soil: Growth of saprotrophic fungi and bacteria in soil journal April 2011
Root penetration in deep soil layers stimulates mineralization of millennia-old organic carbon journal September 2018
Shifting from a fertilization-dominated to a warming-dominated period journal September 2017
A physiological method for the quantitative measurement of microbial biomass in soils journal January 1978
The bioelements, the elementome, and the biogeochemical niche journal March 2019
A new conceptual model on the fate and controls of fresh and pyrolized plant litter decomposition journal February 2015
Comparison of factors limiting bacterial growth in different soils journal October 2007
Nitrogen Additions and Litter Decomposition: a Meta-Analysis journal December 2005
A total quasi-steady-state formulation of substrate uptake kinetics in complex networks and an example application to microbial litter decomposition journal January 2013
Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest journal August 2011
Global trends in senesced-leaf nitrogen and phosphorus journal September 2009
Reconsidering the phosphorus limitation of soil microbial activity in tropical forests journal February 2018
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed journal February 2008
Stability of organic carbon in deep soil layers controlled by fresh carbon supply journal November 2007
The human-induced imbalance between C, N and P in Earth's life system journal October 2011
Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling journal April 2013
Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil journal August 2014
Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling journal April 2014
Soil microbial CNP and respiration responses to organic matter and nutrient additions: Evidence from a tropical soil incubation journal July 2018