Rhizosphere interactions under elevated CO2: Impact on soil organic carbon dynamics

Shuijin HuNorth Carolina State University

Raleigh, NC 27695Email: shuijin_hu@ncsu.edu

Plant-Microbe Interactions

Microbial responses to climate change

Carbon & nitrogen dynamics in agroecosystems

Microbes & plant competition

Microbial diversity & ecosystem stability

An Overview of Recent and Ongoing Research Projects

Air temperature has increased ca. 0.6 oC

Air temperature is predicted to increase another 2-5 oC in the

next 100 years

The increasing atmospheric CO2 is correlated with the temperature rise

Global warming has some major

consequences

Global climate change: Atmospheric CO2 has been increasing since the Industrial Revolution

One central goal of global change research is to understand:

whether and how terrestrial ecosystems can sequester more organic C.

Why ecosystem C sequestration for mitigation of climate change?

1. Air CO2-C: 750 × 1015 g

2. Biomass-C: 550-650 × 1015 g

3. Soil organic C: 1500-2100 × 1015 g

Active C pools on the Earth surface:

Elevated CO2 stimulates photosynthesis and net primary production – Increases short-term C inputs

Herrick & Thomas. 2001

Prerequisites for long-term ecosystem C sequestration under elevated CO2

1. Plants can effectively acquire available nutrients;

2. Mechanisms exist to sustain N supply for plants;

3. Microbial decomposition is “contained”.

Plants are primarily nutrient-limited but microbes are C-limited

1. Can plants acquire available nutrients more effectively under elevated CO2?

The prevailing paradigm in 1990’s was:

Microbes outcompete plants for acquiring nutrients in soil.

Microbes

Elevated CO2

Plants

Available N

Organic N

C inputs

Elevated CO2 alters the plant-microbial competition in favor of plant N utilization.

Hu et al. 2001. Nature

Luo et al. 2004. Bioscience

Nutrient Limitation of Ecosystem C Sequestration

2. Are there mechanisms that sustain N supply for plants under elevated CO2?

Can CO2-stimulation of plant growth be sustained

over time?

To a large degree, it will depend on whether plants can acquire sufficient nutrients from the organic pool.

Elevated CO2

Plants

Microbes

Available N

Organic N

C inputs

+ Elevated CO2 increased plant N acquisition from soil organic N pool.

Hu et al. 2005. Global Ch. Biol.Zak et al. 2011. Ecology Letters.Drake et al. 2011. Ecology Letters

The Summary

Plants are more effective in nutrient acquisition under elevated than ambient CO2.

Next Question

How does elevated CO2 increase plant nutrient acquisition from soil?

How does elevated CO2 increase plant nutrient acquisition from soil?

Plants are more effective in nutrient acquisition under elevated than ambient CO2.

How does elevated CO2 increase plant nutrient acquisition from soil?

The Summary

Plants are more effective in nutrient acquisition under elevated than ambient CO2.

How does elevated CO2 increase plant nutrient acquisition from soil?

NO3–

NO3–

NO3–

NH4+

Ca2+

K+

PO43-

Mg2+

Residues

PO43-

(15NH4)2SO4

bacteria

fungi

Elevated CO2

Hu et al. 2005, Global Change Biol.

Indeed, one major finding over the last two decades is: Elevated CO2 increases soil fungi,

particularly mycorrhizal fungi.

Then the question is:

Why?

Treseder, 2004. New Phytologist

1. Mycorrhizae are symbiotic associations between plant roots and fungi;

2. Over 80% of terrestrial plants form mycorrhizae with fungi;

3. Plants allocate up to 20% of photosynthates to mycorrizal fungi under ambient CO2 and up to 35-40% under elevated CO2.

Ectomycorrhzae Arbuscular Mycorrhizae

AM fungi protect organic C from microbial attack

Scanning electron micrograph of a VA mycorrhizal fungus with particles of clay firmly attached (left) and VA mycorrhizal fungi binding microaggregates into a stable macroaggregate (Tisdall and Oades 1979).

The current paradigm of elevated CO2 impact on soil C

Rillig et al., 1999, Nature; Treseder & Allen, 2000, New Phytol.Antoninka et al. 2009, GCB. Wilson et al. 2009. Ecol. Letters

Elevated CO2

Plant Growth

Soil Aggregation

Mycorrhizae

Extraradical Fungal Hyphae

Cell Wall Materials (Chitin)

Carbon Sequestration

GlomalinPolysaccharides

Major issues related to the current paradigm

1. The current paradigm is largely based on correlative information, rather than direct evidence;

2. Emerging evidence suggests that AM fungi may increase decomposition of organic residues (Hodge et al. 2001, Nature; PNAS 2010; Tu et al. 2006, Global Change Biology).

Hodge et al. 2001

Can CO2-stimulation of AM fungi increase decomposition of organic matter in soil?

Five steps to assess the impact of CO2–enhancement of AM fungi on organic C

decomposition

CSTR chambers

Step 1

A microcosm experiment to assess AMF-mediated organic C decomposition under different CO2 and N levels

Microcosm unit

Fig. 7 Root- and hyphal-ingrowth cores

Nylon net(1.6 mm)

Nylon mesh(20 µm )

Fig. 7 Root- and hyphal-ingrowth cores

Nylon net(1.6 mm)

Nylon mesh(20 µm )

13C/15N labeled materials

Isolation of root contribution from fungal effects on organic C decomposition

Step 2A microcosm experiment to examine the impact of AMF

identity on AMF-mediated organic C decomposition under different CO2 levels

AM fungal species or assemblages

A. Acaulospora morrowiae

B. Gigaspora margarita

C. Glomus clarum

D. Assemblage A: The combination of A, B and C

F. Assemblage B: Eight species from field, including A, B & C

Step 3 A field experiment to determine AMF-mediated

organic C decomposition under elevated CO2

Open-top chambers used to simulate atmospheric CO2 concentrations under future climate scenarios

Elevated CO2 increased mycorrhizal infection of roots and AMF biomass in soil

Fig. S3. Elevated CO2 stimulated the growth of AMF in roots of Avena fatua and wheat, and in soil

Result 1:

Result 2: Higher AMF under elevated CO2 increases decomposition

Cheng et al. 2012. ScienceA: Microcosm Exp. 1; B. Microcosm Exp. 2;C. Field Exp.

Why does elevated CO2 concentration increase organic C decomposition?

Our initial hypothesis was:

Elevated CO2 stimulates organic C decomposition because 1. N becomes more limiting, 2. plants under elevated CO2 need to obtain more N, and 3. plants allocate more carbohydrates to prime

decomposition through stimulating saprotrophs.

Does elevated CO2 really reduce N availability?

Result 3:

Elevated CO2 reduces soil NH4+ in N-limiting soils but

increases soil NO3- in the N-rich field soil

Cheng et al. 2012. Science

A: Microcosm Exp. 1; B. Microcosm Exp. 2;C. Field Exp.

These results led us to ask: 1. Why do plants not use the increased NO3

- under elevated CO2?

2. Does elevated CO2 lead to plant preference of soil NH4

+ over soil NO3- ?

Bloom et al. 2010. Science

Fig. 1. Three methods for assessingnitrate absorption (Absorb) and assimilation (Assim.) in wheatand Arabidopsis plants in hydroponic solutions where the shoots were exposed to atmospheres containing 380-ppm CO2 and 21% O2, 720-ppm CO2 and 21% O2, or 380-ppm CO2 and 2% O2.

Does elevated CO2 lead to plant preference of soil NH4

+ over soil NO3- ?

Step 4

A meta-analysis of elevated CO2 impact on soil N and plant N acquisition in the literature

Step 4

A meta-analysis of elevated CO2 impact on soil N and plant N acquisition in the literature.

1. 38 studies that quantified the concentrations of soil NH4

+ and NO3– and/or the capacity of plant use of NH4

+ and NO3

– under eCO2;

2. These studies encompassed more than 58 species of crop, grass, and tree species.

Result 4:

Elevated CO2 reduced plant NO3- uptake and

increased soil NO3- (Net effect %).

Cheng et al. 2012. Science

20

40

-20

-40

Step 5

A field experiment to assess the impact of nitrification inhibition on AMF-mediated organic C decomposition under elevated CO2

X

Result 5:Inhibition of nitrification offsets CO2-enhancement of

AMF-mediated organic C decomposition

Cheng et al. 2012. Science

The Summary

Fig. 4. A conceptual frameworkof AMF-mediated decompositiondriven by CO2-enhancement of plant N acquisition. CO2-enhancement of AMF primes residue decomposition and ammonium (NH4

+) releaseand optimizes NH4

+ acquisition, while reducing nitrification.

Cheng et al. 2012. Science

Potential Implications

1.The contribution of arbuscular mycorhizal fungi to soil C sequestration under future CO2 scenarios may have been over-estimated;

2.Increasing plant N use efficiency and reducing decomposition through effective management of soil N transformations are keys to facilitate soil C sequestration.

Acknowledgements

Lab members (in the last 6 years): Sean Blosvies*, Xin Chen, Jared Chauncey, Lei Cheng, Mary Claire Garrison, Natalie Gross*, Anna Johnson, Marissa Lee, Lingli Liu, Karen Parker, Tomin Sa*, Qinghua Shi*, Cong Tu*, Jinping Wang*, Liang Wang, Yi Wang, Dolly Watson, Scotty Wells*, Li Zhang*, Yi Zhang*, Lishi Zhou*

Major CollaboratorsNCSU: David Shew, Chris Reberg-Horton, Julie Grossman, Frank Louws, Mike Benson,

David Bird, Mike Burton, Nancy Creamer, Marc Cubeta, Ralph Dean, Greg Hoyt, Paul Mueller, Jean Ristaino, David Ritchie, Tom Rufty, Michelle Schroeder, Wei Shi, Lane Tredway, Dolly Watson

USDA-ARS: Fitz Booker, Kent Burkey

Funding Agencies: USDA-NRI: Soil Processes, Pest Management Alternative, Managed EcosystemsUSDA-SAREUSDA_NIFA_ORGNC Center for Turfgrass Environmental Research & EducationUSDA-ARS Plant Research Unit