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Breathtaking – extracellular respiration in soil

A fraction of the enzymes in soil microorganisms, released when the latter die, migrate to soil particles and re-initiate the process of respiration. The discovery of this kind of extracellular metabolism marks a turning point in research in this field. It also reveals that microorganisms are not the only element responsible for the decomposition of organic matter in soil and the release of carbon into the atmosphere. We interviewed Sébastien Fontaine at INRA – Clermont-Ferrand.

Experiment set up in 1928. Detail of plot n°24: addition of slag, which prevents soil acidification and improves soil structure. The structure remains cloddy facilitating water infiltration.. © INRA, WEBER Jean
By Louise Bergès, translated by Emma Morton-Saliou
Updated on 10/14/2013
Published on 09/10/2013

How did you discover this surprising phenomenon?

Photographic images of microbial cells before and after exposure of soil to 45 kGy gamma irradiation. The black dash represents 500 nm.. © Université de Clermont Ferrand, Jonathan Colombet
Photographic images of microbial cells before and after exposure of soil to 45 kGy gamma irradiation. The black dash represents 500 nm. © Université de Clermont Ferrand, Jonathan Colombet

 Sébastien Fontaine: By accident! While studying soil fungi, we discovered CO₂ emissions in irradiated soil – which contains no microorganisms. We realised that respiration was occurring in the absence of living cells. We refer to the process as ‘Exomet’: ‘exo’ meaning outside the cell, and ‘met’ meaning metabolism.

Until now, it was thought that respiration could only occur in an intracellular environment in which enzymes are protected inside cellular compartments in specific physical and chemical conditions. These enzymes are responsible for glycolysis and the citric acid, (or Kreb’s) cycle – two key oxidative processes.

How does Exomet occur?

 S. F.: Soil microorganisms release the content of their cells into the surrounding environment when they die. These molecules, including the enzymes involved in respiration, are in contact with soil particles. A small fraction (5-10%) of these enzymes will connect with minerals or humus to reconstitute a meta-organism capable of producing the cascade of chemical reactions which occur in respiration.

We recreated an Exomet in our lab using a large quantity of yeast cells, and observed rapid and intense levels of CO₂ emissions six hours following exposure to the soil.

We don’t know what the exact structure of this metabolism is, but we believe that the molecular exchanges occur at random. Enzymes and their substrates are concentrated within soil particles, thus increasing the likelihood of a chemical reaction. Substrate flows between enzymes, on the other hand, occur via diffusion.

What role does soil play?

 S. F.: Soil particles play a major role in protecting enzymes from respiration. Free enzymes decompose within a few hours, but an Exomet can be maintained in the soil over several hundred days!

We observed this kind of extracellular respiration in every type of soil we tested. Quantities of CO₂ emissions varied between the different soils, however.

Soils from around the world, tested for the presence of Exomet (extracellular respiration).. © INRA, Sébastien Fontaine
Soils from around the world, tested for the presence of Exomet (extracellular respiration). © INRA, Sébastien Fontaine
 

Although we cannot make any generalisations for the moment, it appears that the texture and pH of a soil affect the intensity of the Exomet: the finer the soil particles, the more the enzymes appear to be stabilised by absorption, and the better the extracellular respiration. Enzymes involved in respiration also function at optimal levels at specific pH levels: more basic environments for glycolysis enzymes and a more acidic environment for citric acid cycle enzymes. In pH-balanced (6-8) soils, both groups of enzymes appear to function well.

In addition, this link to soil particles makes the metaorganism resistant to high temperatures and high pressure. It is not altered when soil samples are heated to normal pasteurisation levels (137 and 150°C), while cells could not survive these conditions. This property could lead to biotechnology applications.

What are the implications of this discovery?

 S. F.: We observed that the Exomet produces between 16 and 48% of all soil-based CO₂ emissions, which suggests that this metabolism is an important determinant in major biogeochemical cycles.

 Exomet resistance to high temperatures could, in the context of global warming, contribute to changes in existing balances in the carbon cycle (1). A balance exists between respiration and photosynthesis (the fixation of atmospheric carbon by plants). During a heat wave, most of the enzymes involved in photosynthesis cease to function at 40°C, while those involved in respiration continue to function due to Exomet. With repeated heatwaves expected in the future (2), an increase in ecosystem CO₂ emissions can be expected.

Where does your research go from here?

 S. F.: Our research is ongoing to ascertain the exact chemical architecture of this metabolism by studying chemical intermediates. Studies of other environments – aquatic ones, for example – and other metabolic processes such as anaerobic digestion are also underway. The only things needed to form an Exomet are the death of microorganisms and the stabilisation by molecules of respiration enzymes, so it’s very likely that the phenomenon is widespread in nature!

(1) The Department of Geology and Geological Engineering of the Université Laval (Quebec, Canada) provides a detailed explanation of how the carbon cycle works (in French)
(2) According to 2007 climate scenarios published by the Intergovernmental Panel on Climate Change (IPCC).

Contact(s)
Scientific contact(s):

Associated Division(s):
Forest, Grassland and Freshwater Ecology
Associated Centre(s):
Auvergne Rhône-Alpes

References

These findings were presented in Minneapolis as part of a guest presentation at the Ecological society of America (ESA) Annual Meeting (4-9 August 2013).

They were also discussed and published in Biogeosciences:

- Maire, V., Alvarez, G., Colombet, J., Comby, A., Despinasse, R., Dubreucq, E., Joly, M., Lehours, A.-C., Perrier, V., Shahzad, T., and Fontaine, S. 2012. An unknown respiration pathway substantially contributes to soil CO2 emissions, Biogeosciences Discuss.,9, 8663-8691, doi:10.5194/bgd-9-8663-2012.

- Maire, V., Alvarez, G., Colombet, J., Comby, A., Despinasse, R., Dubreucq, E., Joly, M., Lehours, A.-C., Perrier, V., Shahzad, T., and Fontaine, S.  An unknown oxidative metabolism substantially contributes to soil CO2 emissions, Biogeosciences, In press.

Partners:

- The Genomes and Environment Microorganism Laboratory (Laboratoire Microorganismes: Génomes et Environnement) at Université Blaise Pascal in Clermont-Ferrand. http://www.lmge.univ-bpclermont.fr/

- VetAgro Sup, (Clermont-Ferrand campus). http://www.vetagro-sup.fr/

- VetAgro Sup, (Montpellier campus), UMR 1208 IATE. http://www.supagro.fr/web/

An additional link in the process of how life appeared on earth

It has been proven that the first complex molecules were produced by certain physical phenomena such as lightning. Concentrated and polymerised in the soil, these molecules produced the first proteins. The discovery of Exomet demonstrates that these proteins and enzymes can arrange themselves in the soil to reconstitute a metabolism as complex as respiration. Researchers hypothesise that an encapsulation mechanism of this metabolism created the first cell forms, contributing to a better understanding of how life first appeared on earth.