An unknown oxidative metabolism substantially contributes to soil CO<sub>2</sub> emissions

Abstract

Abstract. The respiratory release of CO2 from soils is a major determinant of the global carbon cycle. It is traditionally considered that this respiration is an intracellular metabolism consisting of complex biochemical reactions carried out by numerous enzymes and co-factors. Here we show that the endoenzymes released from dead organisms are stabilised in soils and have access to suitable substrates and co-factors to permit function. These enzymes reconstitute an extracellular oxidative metabolism (EXOMET) that may substantially contribute to soil respiration (16 to 48% of CO2 released from soils in the present study). EXOMET and respiration from living organisms should be considered separately when studying effects of environmental factors on the C cycle because EXOMET shows specific properties such as resistance to high temperature and toxic compounds.

Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: 13C metabolic tracing reveals the mechanisms

“…Previously, persistent CO 2 release from soil with eliminated or inhibited respiration was attributed to abiotic processes (Rozycki and Bartha, 1981;Trevors, 1996) and extracellular oxidative metabolism (Maire et al, 2013). Our data clearly demonstrate that inhibition of electron transport chain cannot stop intracellular glucose metabolism: microorganisms circumvent respiration inhibition via temporary extracellular electron transfer, giving organisms a chance to reconstruct new electron transport chains and resume normal (aerobic) respiration.…”

“…Increased 13 C recovery and reduced total CO 2 after NaN 3 inhibition could not be explained by a shift towards fermentative metabolism resulting from respiration inhibition, as 13 CO 2 from fermentation would be C-4 dominated instead of C-1. High CO 2 emission from soils with minimized microbial activity can be attributed to release of active oxidative extracellular enzymes (EXOMET) from dead organisms (Maire et al, 2013). To prove or reject the relevance of EXOMET compared with cellular metabolism, investigation of intracellularly formed metabolites (that is, de novo formed microbial biomass) was conducted.…”

“…This cannot be attributed to errors in CO 2 determination caused by formation of volatile hydrazoic (HN 3 ) acid (Rozycki and Bartha, 1981;Trevors, 1996), as chloroform fumigation also results in persistent CO 2 emission (Voroney and Paul, 1984;Blankinship et al, 2014). The CO 2 emitted from soil following microbial metabolic inhibition was previously ascribed to active oxidative extracellular enzymes (EXOMET) already present in soil or released from dead cells (Maire et al, 2013). However, since this study solely traced catabolism, the ultimate source of the emitted CO 2 could not be definitively concluded.…”

“…Increased glucose oxidation after pyruvate formation also accounts for the altered pattern of 13 C recovery observed in bulk soil, with even stronger decrease in C-4 and C-2 incorporation at day 1 compared with control soil . Intracellular transformation of glucose after NaN 3 inhibition opposes the concept of extracellular oxidative metabolism (Maire et al, 2013), as surviving microbes must be responsible for the observed transformation. The ≈3-fold lower 13 C recovery in microbial biomass and higher recovery in CO 2 following inhibition compared with control conditions (Figure 1 and 2, bottom) imply that the surviving microbes utilized substantial amount of glucose for energy production.…”

Disentangling the rates of carbonyl sulphide (COS) production and consumption and their dependency with soil properties across biomes and land use types

“…The amount of liquid water required for maintaining such biological activity, including thiocyanate hydrolase activity, could be extremely small and still result in a detectable amount of COS 30 emitted. In addition, Maire et al (2013) showed that endoenzymes released from dead organisms were stabilised in soils and could still lead to extracellular oxidative metabolism. This could also partly explain the continuation of COS production even at very low water content in our soils.…”