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An Unknown Oxidative Metabolism Substantially Contributes to Soil CO2

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An Unknown Oxidative Metabolism Substantially Contributes to Soil CO2 EGU Journal Logos (RGB) Open Access Open Access Open Access Advances in Annales Nonlinear Processes Geosciences Geophysicae in Geophysics Open Access Open Access Natural Hazards Natural Hazards and Earth System and Earth System Sciences Sciences Discussions Open Access Open Access Atmospheric Atmospheric Chemistry Chemistry and Physics and Physics Discussions Open Access Open Access Atmospheric Atmospheric Measurement Measurement Techniques Techniques Discussions Open Access Biogeosciences, 10, 1155–1167, 2013 Open Access www.biogeosciences.net/10/1155/2013/ Biogeosciences doi:10.5194/bg-10-1155-2013 Biogeosciences Discussions © Author(s) 2013. CC Attribution 3.0 License. Open Access Open Access Climate Climate of the Past of the Past Discussions An unknown oxidative metabolism substantially contributes to soil Open Access Open Access Earth System CO2 emissions Earth System Dynamics 1,* 1,2 3 1 4 5 Dynamics1 3 V. Maire , G. Alvarez , J. Colombet , A. Comby , R. Despinasse , E. Dubreucq , M. Joly , A.-C. Lehours , Discussions V. Perrier5, T. Shahzad1,**, and S. Fontaine1 1INRA, UR 874 UREP, 63100 Clermont-Ferrand, France Open Access Open Access 2Clermont Universite,´ VetAgro Sup, 63000, Clermont-Ferrand, France Geoscientific Geoscientific 3University of Clermont Ferrand, UMR 6023 LMGE, 63177 Aubiere,` France Instrumentation Instrumentation 4INRA, UMR 1095 UBP, 63100 Clermont-Ferrand, France Methods and Methods and 5Montpellier SupAgro, UMR 1208 IATE, 34060 Montpellier, France *present address: Department of Biological Sciences, Macquarie University, NSW 2109, AustraliaData Systems Data Systems **present address: Department of Environmental Sciences, Government College University Faisalabad, Discussions Open Access Open Access 38000-Allama Iqbal Road Faisalabad, Pakistan Geoscientific Geoscientific Correspondence to: S. Fontaine ([email protected]) Model Development Model Development Discussions Received: 31 May 2012 – Published in Biogeosciences Discuss.: 18 July 2012 Revised: 25 January 2013 – Accepted: 27 January 2013 – Published: 21 February 2013 Open Access Open Access Hydrology and Hydrology and Abstract. The respiratory release of CO2 from soils is a ma- lysts. For instance, the physicalEarth oxidation System of one molecule of Earth System jor determinant of the global carbon cycle. It is traditionally glucose requires a temperature greater than 500 ◦C. In soils, considered that this respiration is an intracellular metabolism microorganisms set up a complexSciences cascade of biochemical re- Sciences consisting of complex biochemical reactions carried out by actions mediated by numerous enzymes making the oxidisa- Discussions Open Access numerous enzymes and co-factors. Here we show that the tion of organic C possible at low temperature. Open Access endoenzymes released from dead organisms are stabilised in The mineralisation of organic C requires two main steps. Ocean Science soils and have access to suitable substrates and co-factors to First, microorganismsOcean secrete extracellular Science enzymes in soil Discussions permit function. These enzymes reconstitute an extracellular in order to deconstruct plant and microbial cell walls (e.g., oxidative metabolism (EXOMET) that may substantially con- endoglucanase), depolymerize macromolecules (e.g., perox- tribute to soil respiration (16 to 48 % of CO2 released from ydase), and ultimately produce soluble substrates for micro- Open Access Open Access soils in the present study). EXOMET and respiration from liv- bial assimilation (e.g., glucosidase) (Chrost,´ 1991; Burns and ing organisms should be considered separately when study- Dick, 2002; Sinsabaugh et al., 2009). No molecule of CO2 is Solid Earth Solid Earth ing effects of environmental factors on the C cycle because released during this depolymerization step. The second step Discussions EXOMET shows specific properties such as resistance to high of mineralisation, during which C is released as CO2, implies temperature and toxic compounds. the absorption and utilisation of solubilized substrates by mi- crobial cells with the aim to produce energy (ATP).Open Access In cells, Open Access soluble substrates are carried out by a cascade of endoen- zymes (enzymes contained by membranes of living cells; The Cryosphere 1 Introduction The Cryosphere Sinsabaugh et al., 2012), along which protons and electrons Discussions are transferred from a substrate to an appropriate acceptor Knowledge of the metabolic pathways through which or- (e.g., the aerobic respiration as well as the anaerobic respira- ganic carbon (C) is oxidised into carbon dioxide (CO2) in tion and the fermentation with different final electron accep- soils is fundamental to understanding the global C cycle and tors; Prescott et al., 2002). Under aerobic conditions, the ox- its interactions with climate (Fontaine et al., 2007; Heimann idative metabolism leads to production of adenosine triphos- and Reichstein, 2008). Organic C is the building block of liv- phate (ATP), consumption of oxygen (O2) and emission of ing organisms and is de facto highly stable in absence of cata- Published by Copernicus Publications on behalf of the European Geosciences Union. 1156 V. Maire et al.: An unknown oxidative metabolism contributes to soil CO2 emissions CO2. Respiration fluxes and ATP production in soils are zymes with glucose in sterilised water and soil. The EXOMET usually positively correlated with activity of dehydrogenase induced by the yeast-extract was quantified by measuring endoenzymes (e.g., Casida et al., 1964), but only some of CO2 and O2 fluxes in water and soil microcosms. Second, them carry a decarboxylase function (e.g., pyruvate dehydro- the protective role of soil particles (minerals and humus) genase, oxoglutarate dehydrogenase) that cut the carboxyl for respiratory enzymes was tested by incubating three en- function of organic C molecules to liberate CO2. zymes involved in glycolysis and the Krebs cycle in five top The function of respiration-carrying endoenzymes de- soils sampled from different regions of the world (Table 1). pends on various co-factors that must be regenerated (e.g., The third part of the manuscript is devoted to the quantifica- + NAD ), on being located adjacent to other enzymes and tion of EXOMET contribution to the CO2 emissions from five on physiological properties of the cell (e.g., redox poten- studied soils. This contribution was quantified with a method tial) (Krebs, 1981; Rich, 2003). Given this complexity and combining modelling and incubations of sterilised and non- the typical fragility of respiratory enzymes, it is tradition- sterilised soils. Finally, we studied some EXOMET properties ally considered that respiration (second step of C minerali- by incubating soils exposed to high temperature, high pres- sation process) is strictly an intracellular metabolism process sure and toxic compounds. (Burns, 1982; Makoi and Ndakidemi, 2008). Besides, from an evolutionary point of view, soil microorganisms have no interest in provoking extracellular respiration since the en- 2 Materials and methods ergy resulting from this respiration (ATP) may escape from the cell that provided enzymes (Allison et al., 2011). How- 2.1 Soil sampling and sterilisation ever, some studies have shown that substantial emission of For each of the five studied sites (Table 1), twenty indepen- CO can persist for several weeks in soils where microbial 2 dent soil samples were collected from the 0–20 cm soil layer. life has been reduced by exposition to toxics (ClCH , or- 3 Soil samples from each site were pooled to make a composite ange acridine) or irradiation to undetectable value (Peterson, sample per site. Soil was sieved at 2 mm and was then used 1962; Ramsay and Bawden, 1983; Lensi et al., 1991; Trevors, to determine pH, texture and organic matter content and to 1996; Kemmitt et al., 2008). Such emission of CO could 2 conduct incubation experiments. The five soils presented tex- not be explained by an activity of surviving microbes that tures from sandy-silted to silty-clay soils, pH ranging from would be present in low quantity in soils, unless considering 4.3 to 8.6 and three types of land use (grassland, forest and unrealistically high cell respiratory activity. Neither could it crops, Table 1). The soil from Theix was used for all inves- be explained by the activity of extracellular enzymes previ- tigations, whereas the other soils were used to generalise the ously secreted by soil microorganisms since these enzymes key findings of this study. only solubilize organic C and do not release CO . To date, 2 Some incubation experiments involved the use of sterilised the cause of CO emission in soils where microbial life has 2 soils. We tested different methods of soil sterilisation (γ - been minimised seems to be unknown and questions our ba- irradiation, autoclaving and dry heating) during preliminary sic knowledge of biology. investigations. Irradiation was chosen among other sterilis- The objective of this study is to understand the cause ing methods for its efficiency to kill soil micro-organisms of CO emission in soils where microbial life has been 2 and for its moderate effect on soil enzymes (see S1 for de- suppressed. We hypothesise that an extracellular oxidative tails of investigations on soil sterilisation). The preservation metabolism (EXOMET) can be reconstituted by respiratory of soil enzymes was important for quantifying the EXOMET endoenzymes released from dead organisms in soils and that contribution to soil CO2 emissions
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