Microbe-iron interactions control lignin decomposition in soil
Introduction
Lignin is one of the most abundant plant-derived organic substances in the terrestrial ecosystems (Boerjan et al., 2003), and its decomposition is critically linked to soil carbon (C) input and persistence. Lignin has long been recognized to limit overall decomposition rate of plant litter due to its perceived biochemical recalcitrance relative to other organic constituents (Talbot and Treseder, 2012). Accordingly, lignin plays a critical role in litter and soil organic C (SOC) decomposition (Parton et al., 1987; Izaurralde et al., 2006). However, a new paradigm of SOC research has challenged the notion and posits that lignin can decompose faster than SOC as a whole (Amelung et al., 2008; Thevenot et al., 2010). Most of the previous studies suggested that lignin decomposition is primarily controlled by fungi and largely regulated by litter chemical properties. Recent work has pointed to the importance of interactions between soil minerals and lignin decomposition to partially reconcile these old and new paradigms (Huang et al., 2019). Yet, fundamental processes that control lignin decomposition are to be understood for evaluating these competing conceptual models. Therefore, it is imperative to develop a generalizable framework to quantify the role of mineral-microbe interactions in lignin decomposition and SOC persistence.
Interactions of lignin and geochemical context, such as iron (Fe) minerals, have been increasingly recognized as key controllers for lignin decomposition (Hall et al., 2015, 2016). Reactive Fe minerals critically influence soil C dynamics through both biotic and abiotic processes (Weber et al., 2006; Kleber et al., 2015). Iron oxides can preferentially associate with aromatic lignin constituents via sorption and coprecipitation to protect lignin C from microbial attack, relative to other organic compounds (Kramer et al., 2012; Riedel et al., 2013). Besides the extracellular oxidative enzymes that are generally considered to break down lignin, reactive oxygen species such as hydroxyl radical generated via Fe redox cycling, known as the Fenton reaction (Hall and Silver, 2013; Hall et al., 2015), can cleave the relatively stable ether bonds of lignin (Wood, 1994; Hammel et al., 2002). Once lignin is depolymerized by these abiotic mechanisms, the lower molecular weight lignin fragments in principle could be readily metabolized by many bacteria in addition to fungi (Cotrufo et al., 2013). Together, Fe minerals exert dual impacts on lignin decomposition: protection of lignin-derived C by Fe oxides (Riedel et al., 2013; Hall et al., 2016; Coward et al., 2018) versus stimulation of lignin decomposition by reactive oxygen species produced via Fe redox cycling in fluctuating redox environments (Hall et al., 2015; Calabrese and Porporato, 2019; Huang et al., 2019).
Although mineral-microbe interactions have been widely understood to control lignin decomposition (Ginn et al., 2017; Calabrese and Porporato, 2019; Zheng et al., 2019; Huang et al., 2021), we still lack a generalizable framework to quantify these interactions that help estimate fates of lignin C and quantify contribution of lignin to SOC persistence. To develop the framework, we need comprehensive data sets to test alternative models regarding the role of mineral-microbe interactions. The study by Huang et al. (2019) employed a C stable isotope approach to distinguish the source of respired CO2 and applied a single anaerobic event of varying duration to generate differences in Fe(II) at the beginning of the incubation. The data set includes high frequent measurements of lignin decomposition over ∼1-yr incubation period (Huang et al., 2019). Interestingly, lignin decomposition rates reached different peaks several months after redox pre-treatments, which may indicate the strong interactions of Fe and lignin. The observed non-linear patterns clearly did not follow traditional first-order kinetics, which has been widely used to describe decomposition of litter and SOC (Parton et al., 1993; Bondeau et al., 2007; Adair et al., 2008; Clark et al., 2011; Koven et al., 2013). Sufficient incubation time and intensive observation data provide strong support for the construction and theoretical analysis of a new framework for lignin decomposition. Indeed, the pattern of lignin decomposition reported in Huang et al. (2019) was also observed in many other soils (Hall et al., 2020). Thus, a framework that is developed based on the data set in Huang et al. (2019) is likely to be applicable to other studies on lignin decomposition, especially in Fe-rich soils.
This study reveals likely mechanisms underlying lignin decomposition via microbe-Fe interactions based on a data-model synthesis of results from an experiment published by Huang et al. (2019). We first evaluated alternative mechanisms as expressed in process-based models, such as first-order kinetics in a multi-pool model, microbially mediated reaction in a Michaelis-Menten model, and microbe-Fe-mediated lignin decomposition as in a microbe-Fe interaction (MiFe) Model. The MiFe model incorporates Fe-mediated breakdown of macromolecular to small molecular lignin C via the Fenton reaction, microbial decomposition of small molecular lignin C, and protection of lignin C via Fe association (Fig. 1). Our evaluations indicated that neither the classical three-pool, first-order kinetics model nor the Michaelis-Menten model well represents the observed patterns of lignin decomposition in Huang et al. (2019) (Fig. 2). In contrast, our new MiFe model better reproduced the observed data (Fig. 2), and was the primary focus of this study. We interpreted modeling results to examine possible key controlling mechanisms and fates of lignin C in soil.
Section snippets
Incubation data
The data used in this study were from an incubation study by Huang et al. (2019). In that incubation study, soil was sampled from an upland valley in a perhumid tropical forest near the El Verde field station of the Luquillo Experimental Forest (18°17′N, 65°47′W), Puerto Rico. This soil is an Oxisol developed from basaltic to andesitic volcaniclastic sediments (pH = 5.03). Soil organic carbon at 0–10 cm measured 44.8 mg g−1, and soil nitrogen was 4.1 mg g−1. The soil at 0–10 cm had 10% sand,
Mechanisms underlying lignin C decomposition
This study identified the microbe-Fe interactions as represented in the MiFe model as the most parsimonious mechanism that can adequately reproduce the dynamic changes of CO2 production from lignin decomposition in all four anaerobic pre-treatments (Fig. 2). In the incubation experiment, soil was pre-treated with 12, 8, 4, or 0 days of anaerobic conditions during the first 12 days and was in an aerobic incubation for subsequent 317 days. These pre-treatments are hereafter termed 12-day, 8-day,
Discussion
Building upon the representative dataset from Huang et al. (2019), our data-model integration proposed a new lignin decomposition framework, which revealed the underlying mechanisms controlling the temporal dynamics of lignin decomposition and lignin fate in soils. Such dynamics are not easily measurable in laboratory studies. Different from the study by Huang et al. (2019), our modeling results clearly demonstrated the progressive patterns of how lignin C was metabolized by microbes and
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
This work is supported by the National Key Research and Development Program of China (2020YFA0607900, 2020YFA0608003) and the National Natural Science Foundation of China (42125503, 42075137). The authors greatly appreciate the constructive comments by Dr. Steven Hall. Contributions from YL to this work was financially supported by US National Science Foundation (DEB 1655499, DEB 2017884), US Department of Energy (DE-SC0020227), and the subcontracts 4000158404 and 4000161830 from Oak Ridge
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The authors contributed equally to this study.