1. North Carolina State University
Rhizosphere interactions under elevated CO2: Impact on soil organic carbon dynamics
Shuijin Hu
North Carolina State University
Raleigh, NC 27695

2. An Overview of Recent and Ongoing Research Projects
Plant-Microbe Interactions
Microbial responses to climate change
Carbon & nitrogen dynamics in agroecosystems
Microbes & plant competition
Microbial diversity & ecosystem stability

3. Air temperature has increased ca. 0.6 oC
Air temperature is predicted to increase another 2-5 oC in the next 100 years

4. The increasing atmospheric CO2 is correlated with the temperature rise

5. Global warming has some major consequences

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

7. One central goal of global change research is to understand:
whether and how terrestrial ecosystems can sequester more organic C. 7

8. Why ecosystem C sequestration for mitigation of climate change?
Active C pools on the Earth surface:
Air CO2-C: × 1015 g
2. Biomass-C: × 1015 g
Soil organic C: × 1015 g

9. Elevated CO2 stimulates photosynthesis and net primary production –
Increases short-term C inputs
Herrick & Thomas. 2001

10. Prerequisites for long-term ecosystem C sequestration under elevated CO2
Plants can effectively acquire available nutrients;
Mechanisms exist to sustain N supply for plants;
Microbial decomposition is “contained”.
Plants are primarily nutrient-limited but microbes are C-limited

11. 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.
In other words, does this soluble N end up more in plants or in microbes?

12. Elevated CO2 Plants Available N Organic N Microbes
C inputs
In other words, does this soluble N end up more in plants or in microbes?
Elevated CO2 alters the plant-microbial competition in favor of plant N utilization.
Hu et al Nature

13. Nutrient Limitation of Ecosystem C Sequestration
Luo et al Bioscience

14. 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.
In other words, does this soluble N end up more in plants or in microbes? 14

15. Elevated CO2 Plants + Available N Organic N Microbes
C inputs +
In other words, does this soluble N end up more in plants or in microbes?
Elevated CO2 increased plant N acquisition from soil organic N pool.
Hu et al Global Ch. Biol.
Zak et al Ecology Letters.
Drake et al Ecology Letters 15

16. The Summary The Summary Next Question
Plants are more effective in nutrient acquisition under elevated than ambient CO2.
Plants are more effective in nutrient acquisition under elevated than ambient CO2.
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?
How does elevated CO2 increase plant nutrient acquisition from soil?
How does elevated CO2 increase plant nutrient acquisition from soil?

17. Elevated CO2 (15NH4)2SO4 NO3– bacteria fungi Ca2+ Residues K+ NH4+
PO43-
Mg2+
Residues
(15NH4)2SO4
bacteria
fungi
Elevated CO2
We further examined plant 15N conc. In the nutrient-poor soil, 15N conc decreased under elevated CO2, but plant 15N conc increased in the nutrient-rich soil, corresponding to a comparable decrease in soil 15N.
Hu et al. 2005, Global Change Biol. 17

18. Indeed, one major finding over the last two decades is: Elevated CO2 increases soil fungi, particularly mycorrhizal fungi.
Then the question is:
Why?
Treseder, New Phytologist

19. Ectomycorrhzae
Arbuscular Mycorrhizae
Mycorrhizae are symbiotic associations between plant roots and fungi;
Over 80% of terrestrial plants form mycorrhizae with fungi;
Plants allocate up to 20% of photosynthates to mycorrizal fungi under ambient CO2 and up to 35-40% under elevated CO2.

20. 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). 20

21. of elevated CO2 impact on soil C
The current paradigm
of elevated CO2 impact on soil C
Elevated CO2
Plant Growth
Soil Aggregation
Mycorrhizae
Extraradical
Fungal Hyphae
Cell Wall Materials (Chitin)
Carbon Sequestration
Glomalin
Polysaccharides
Rillig et al., 1999, Nature; Treseder & Allen, 2000, New Phytol.
Antoninka et al. 2009, GCB. Wilson et al Ecol. Letters

22. Major issues related to the current paradigm
The current paradigm is largely based on correlative information, rather than direct evidence;
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).

23. Hodge et al. 2001

24. 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

25. Step 1 A microcosm experiment to assess AMF-mediated organic
C decomposition under different CO2 and N levels
CSTR chambers
Microcosm unit

26. Isolation of root contribution from fungal effects on organic C decomposition
13C/15N labeled materials

27. Step 2
A 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

28. 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

29. Result 1:
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

30. Higher AMF under elevated CO2 increases decomposition
Result 2:
Higher AMF under elevated CO2 increases decomposition
A: Microcosm Exp. 1;
B. Microcosm Exp. 2;
C. Field Exp.
Cheng et al Science

31. 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, 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?

32. Result 3:
Elevated CO2 reduces soil NH4+ in N-limiting soils but increases soil NO3- in the N-rich field soil
A: Microcosm Exp. 1;
B. Microcosm Exp. 2;
C. Field Exp.
Cheng et al Science

33. These results led us to ask:
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- ?

34. Fig. 1. Three methods for assessing
nitrate absorption (Absorb) and assimilation (Assim.) in wheat
and 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.
Bloom et al Science

35. Step 4
A meta-analysis of elevated CO2 impact on soil N and plant N acquisition in the literature
Does elevated CO2 lead to plant preference of soil NH4+ over soil NO3- ?

36. Step 4
A meta-analysis of elevated CO2 impact on soil N and plant N acquisition in the literature.
38 studies that quantified the concentrations of soil NH4+ and NO3– and/or the capacity of plant use of NH4+ and NO3– under eCO2;
These studies encompassed more than 58 species of crop, grass, and tree species.

37. Result 4:
Elevated CO2 reduced plant NO3- uptake and increased soil NO3- (Net effect %). 20 40
-20
-40
Cheng et al Science

38. Step 5
A field experiment to assess the impact of nitrification inhibition on AMF-mediated organic C decomposition under elevated CO2 X

39. Result 5:
Inhibition of nitrification offsets CO2-enhancement of AMF-mediated organic C decomposition
Cheng et al Science

40. The Summary Fig. 4. A conceptual framework
of AMF-mediated decomposition
driven by CO2-enhancement of plant N acquisition. CO2-enhancement of AMF primes residue decomposition and ammonium (NH4+) release
and optimizes NH4+ acquisition, while reducing nitrification.
Cheng et al Science

41. Potential Implications
The contribution of arbuscular mycorhizal fungi to soil C sequestration under future CO2 scenarios may have been over-estimated;
Increasing plant N use efficiency and reducing decomposition through effective management of soil N transformations are keys to facilitate soil C sequestration.

42. 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 Collaborators
NCSU: 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 Ecosystems
USDA-SARE
USDA_NIFA_ORG
NC Center for Turfgrass Environmental Research & Education
USDA-ARS Plant Research Unit