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Commentary on 'A role for genetically modified organisms in soil carbon

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Conference Paper · April 2004

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 Commentary on “A role for genetically modified organisms in soil carbon

sequestration”1

R. Michael Miller,

Environmental Research Division

Argonne National Laboratory
Argonne, IL 60439
Present at: “Applications of Biotechnology to Mitigation of Greenhouse Warming”

Proceedings of the St. Michaels Workshop, April 13-15, 2003

Battelle Press

Sponsored by

Pacific Northwest National Laboratory

EPRI

USDOE/OS/BER

1. Miller, M. 2004. Commentary on role of genetically modified soil organisms in soil carbon
sequestration. p. 90-93 In N.J. Rosenberg, F.B. Metting and R.C. Izaurralde (eds.)
Applications of biotechnology to mitigation of greenhouse warming. Proceedings of St.
Michaels II Workshop, 13-15 April 2003, St. Michaels, MD. Battelle Press, Columbus, OH.
213 pp.

The submitted manuscript has been created by

the University of Chicago as operator of Argonne
National Laboratory under Contract No. W-31-
109-ENG-38 with the U.S. Department of
Energy. The U.S. government retains for itself,
and others acting on its behalf, a paid-up,
nonexclusive, irrevocable worldwide license in
said article to reproduce, prepare derivative
works, distribute copies to the public, and
perform publicly and display publicly, by or on
behalf of the government.
Commentary on “A role for genetically modified organisms in soil carbon sequestration”

R. Michael Miller, Argonne National Laboratory

The genetic modification of plant and microbial traits as a means of increasing

carbon sequestration in soils is a technology still in its infancy. The greatest potential for

immediate benefits to soil carbon sequestration will most likely come from research

aimed at modifying plant traits associated with the structure and function of roots and

their influence on rhizosphere organisms, particularly the mycorrhizal symbiosis. I am

not as optimistic about the benefits of using genetically modified microbes as a means for

increasing in situ sequestration; especially if research is conducted in isolation from roots

(the potential benefits though are great). As Rice and Angle have discussed, history has

demonstrated how difficult it is for any introduced microorganism to survive over the

long term in a soil environment.

When the mechanisms controlling soil carbon sequestration are placed in

perspective, it is the amount, quality and location of plant inputs that drive carbon

sequestration in soils. Although primary production is the principal determinant in the

sequestration process, it is the size and activity of the soil’s microbial community that

regulates the sequestration of inputs via the mineralization and immobilization of plant

and microbially derived residues. On a carbon basis, microbial biomass C usually

accounts for between 1 and 4 % of the total soil organic carbon pool, with the exact

amount being dependent upon management practice, edaphic factors, climate, and of

course the amount and quality of plant inputs. Rice and Angle give the view that a

change in cropping and tillage practices could sequester a considerable amount of C

through the buildup of microbial biomass per se. I have no arguments with this premise,

but believe such an approach to be a one-time accounting event. In addition, a potential

negative consequence to greater microbial biomass is that such an increase is usually

associated with a proportional increase in growth and maintenance respiration and, thus,

increased substrate utilization. On the other hand, an increase in substrate utilization may

benefit sequestration by transforming more labile substrates into residues with longer

residence times.

How can the residence time of plant and microbially derived residues be

increased? The mean residence time of a substrate in soil is usually determined by its

biochemical recalcitrance (or degree of biological rendering) and by the extent to which it

is physically or chemically protected from decomposition by association with soil

minerals (Jastrow and Miller, 1998). In general, fungi are able to exploit and use

substrates more efficiently than bacteria. About 50% of substrates metabolized by fungi

end up as biomass. By comparison, 60% of the C metabolized by bacteria is respired

(Hodge et al., 2000). Additionally, fungal cell wall components, such as chitin and

melanin, are more complex and more difficult to decompose than the peptidoglucan

residues derived from bacterial cell walls (Guggenberger et al., 1999). Hence,

management practices that increase the proportion of fungi in the microbial community

should result in more C transferred to more recalcitrant pools compared to the same soil

with a microbial community dominated by bacteria.

When considering soil systems, we need to recognize that the kinds of

microorganisms that proliferate within a given soil depend on whether one is dealing with

“bulk-” or “rhizosphere-” dominated soils. For example, soil that is not immediately
influenced by the activities of roots (i.e., bulk soil) is typically dominated by saprophytic

processes, with the energy driving sequestration derived from the breakdown of plant and

microbial residues, which often may be soluble forms leached from surface residues.

Rhizosphere soils, on the other hand, are soils under the direct influence of living roots.

Hence, rhizosphere-associated microbes have a more direct conduit to photosynthate

carbon as they metabolize organic exudates and sloughed root cells of actively growing

roots in addition to decomposing root detritus. The rhizosphere microbes are also in

direct competition with roots for access to nutrients in soil solution. Rice and Angle,

emphasize that simple genetic differences in a crop species can alter the microbial

population within the rhizosphere. This observation suggests that the kinds of plants we

cultivate potentially could be used as a tool for controlling or at least influencing

microbial processes.

Taken a step further, we need to realize that the cultivars used by modern

agriculture and forestry have been selected for growth under intensive management

practices. This factor becomes especially important when we consider the contributions

of the mycorrhizal symbiosis to carbon sequestration. Rice and Angle emphasize the

importance of this symbiosis where as much as 25 % of a plant’s photosynthate can be

allocated to this important symbiosis (Miller et al., 2002). They further point to the role

played by extraradical hyphae of mycorrhizal fungi to soil structure stabilization and

consequently carbon sequestration (Jastrow and Miller, 1998; Wright and Upadhyaya,

1998). Research in our laboratory indicates that between 2 to 9 % of the annual carbon

input to the soil organic C pool is be derived from the extraradical phase of mycorrhizal

fungi (in preparation). A non-target consequence of modern agriculture crop breeding

practices may be a reduction or loss in the expression of the mycorrhizal responsiveness

trait, colonization, and the concomitant production of a more fibrous morphology root

system (Hetrick et al., 1992). Yet, if we are to gain the full benefit of the genetic capacity

of rhizosphere organisms we will need to take a step back and identify those plant and

microbial traits that may allow for greater carbon sequestration to occur. Those plant

traits that may have the greatest influence on carbon sequestration are most likely those

associated with root morphology and architecture, the production of specific exudates,

and the nature of mycorrhizal associations.

A good example for non-target effects on the mycorrhizal symbiosis has been

demonstrated for modern winter wheat cultivars (those released after 1950) where it

appears that modern cultivars tended to be less responsive to the mycorrhizal symbiosis

than earlier cultivars and ancient land races (Hetrick et al, 1992, 1995). These studies

demonstrated a strong relationship between root morphology and colonization by

mycorrhizal fungi, with a reduction in colonization being associated with an increase in

root fibrousness. It was also demonstrated that the genes for mycorrhizal responsiveness

exist on at least six different chromosomes. Hence, a complicated linkage among the

traits for mycotrophy, colonization and root fibrousness appear to exist in winter wheat.

What is not known is the relationship between these traits and soil carbon sequestration

potential, a relatively unexplored area of biology.

Recent research has demonstrated up regulation of photosynthesis by the

mycorrhizal fungus (Miller et al., 2002). It appears that the mycorrhizal fungus is able to

create its own currency. Thus, mycorrhizal plants can have a greater net carbon gain than

nonmycorrhizal plants (of equivalent size). The upshot is that a significant portion of the
additional photosynthate ends up being allocated to fungal biomass. Since mycorrhizal

fungal cell walls are primarily composed of chitin, the increased photosynthate allocated

to fungal tissue is being placed in a sink that is more recalcitrant than most plant tissues.

As much as we know about the ecology of soils, we are still very much in a

descriptive phase. Furthermore, our ability to manipulate the growth and activities of

groups of organisms in situ is limited, being temporally short and difficult to constrain.

As mentioned by Rice and Angle, our limitations are particularly problematic when

specific groups of microbes are introduced into soils. Hence, one of our great challenges

will be to utilize these organisms in a manner that not only promotes the sequestration of

carbon at a local scale within soils but also enables sequestration to occur across the

landscape.

Hence, enhancement of carbon sequestration in soils will require fundamental

understanding and identification of those components that most control the sequestration

process. If the major controls on C sequestration are microbial, one may refer to genomic

information to enhance the signaling between the plant and the rhizosphere

microorganisms. If the major controls are plant-derived, improved understanding of the

genome may be used to enhance expression of key traits (e.g., production of specific

exudates, alteration of root morphology and architecture, or mycorrhizal associations).

References:

Guggenberger G., Frey S.D., Six J., Paustian K., and Elliott E.T. 1999. Bacterial and

fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil

Science Society America Journal 63:1188-1198.

 Hetrick B.A.D., Wilson G.W.T., and Cox T.S. 1992. Mycorrhizal dependence of

modern wheat varieties, landraces, and ancestors. Canadian Journal of Botany 70:

2032-2040.

Hetrick B.A.D., Wilson G.W.T., Gill B.S., and Cox T.S. 1995. Chromosome location of

mycorrhizal responsiveness genes in wheat. Canadian Journal of Botany 73: 891-

897.

Hodge A., Robinson D., and Fitter A. 2000. Are microorganisms more effective than

plants at competing for nitrogen? Trends in Plant Science 5: 304-308.

Jastrow J.D., and Miller R.M. 1998. Soil aggregate stabilization and carbon

sequestration: Feedbacks through organomineral associations, in Lal, R., Kimble,

J., Follett, R., and Stewart, B. (eds.), pp. 207-223.

Miller R.M., Miller S.P., Jastrow J.D., and Rivetta C.B. 2002. Mycorrhizal mediated

feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii.

New Phytologist 155: 149-162.

Wright S.F., and Upadhyaya A. 1998. A survey of soils for aggregate stability and

glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi.

Plant and Soil 198: 97-107.

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