Enzymes, Manganese, or Iron? Drivers of Oxidative Organic Matter Decomposition in Soils

Abstract

Oxidative decomposition of soil organic matter determines the proportion of carbon that is either stored or emitted to the atmosphere as CO2. Full conversion of organic matter to CO2 requires oxidative mechanisms that depolymerize complex molecules into smaller, soluble monomers that can be respired by microbes. Current models attribute oxidative depolymerization largely to the activity of extracellular enzymes. Here we show that reactive manganese (Mn) and iron (Fe) intermediates, rather than other measured soil characteristics, best predict oxidative activity in temperate forest soils. Combining bioassays, spectroscopy, and wet-chemical analysis, we found that oxidative activity in surface litters was most significantly correlated to the abundance of reactive Mn­(III) species. In contrast, oxidative activity in underlying mineral soils was most significantly correlated to the abundance of reactive Fe­(II/III) species. Positive controls showed that both Mn­(III) and Fe­(II/III) species are equally potent in generating oxidative activity, but imply conventional bioassays have a systematic bias toward Fe. Combined, our results highlight the coupled biotic-abiotic nature of oxidative mechanisms, with Mn-mediated oxidation dominating within Mn-rich organic soils and Fe-mediated oxidation dominating Fe-rich mineral soils. These findings suggest microbes rely on different oxidative strategies depending on the relative availability of Fe and Mn in a given soil environment.

Manganese limitations and the enhanced soil carbon sequestration of temperate rainforests

“…Much of research into peroxidase enzymes has focused on litter layers and organic horizons (Berg et al 2015), but these decay processes in temperate forests clearly extend into mineral soils as well. Jones et al (2020) proposed a useful distinction in oxidative decomposition processes, which would vary between Mn (peroxidases produced by white-rot fungi)…”

“…Empirical models of soil organic carbon (SOC) turnover and sequestration are increasingly recognizing an important role for manganese (Mn 2+ ), which is a co-factor for an enzyme, Mn-peroxidase (MnP), involved in oxidative decomposition of organic matter (Berg et al 2015;Stendahl et al 2017;Keiluweit et al 2015;Jones et al 2020). Mn-peroxidases and other class II secretory fungal peroxidases are produced almost exclusively by fungi from the class Agaricomycete, a large and diverse group that includes both free living saprotrophic and symbiotic ectomycorrhizal species (Morgenstern et al 2008;Floudas et al 2012;Kellner et al 2014).…”

Influences of temperature and moisture on abiotic and biotic soil CO2 emission from a subtropical forest

“…Besides the thermal degradation pathway, the ROSs oxidation pathway could also contribute substantially to the soil abiotic CO 2 emission. As previous studies demonstrated, existence of iron (Fe) and magnesium (Mn) may substantially contribute to soil CO 2 emission via producing ROSs (such as hydroxyl radical and hydrogen peroxide) to oxidize SOC [25][26][27]. The studied soil is a type of highly weathered soil that is rich in the Fe content and contains detectable Mn content [28].…”

“…1 ). Despite the abiotic oxidation potential of Fe and Mn, we also recognize that existence of soil organisms may substantially accelerate the Fe and Mn mediated abiotic oxidation process, since production of Fe (II) and Mn (III) are predominantly regulated by soil microorganisms [ 27 ].…”

Micronutrients in Food Production: What Can We Learn from Natural Ecosystems?

“…The utilization of Mn by fungi and bacteria in forest ecosystems provides some useful insights into the potential issues surrounding the use of microbes for crop biofortification [133][134][135][136]. Manganese plays a key role in litter decomposition by fungi, which typically use Mn for two key functions: as a structural component for lignin-degrading enzymes, such as Mn-peroxidase, and as an electron receiver/donator during the decomposition process [133,137].…”