Plant mixture effects on carbon-degrading enzymes promote soil organic carbon accumulation

Highlights

• Plant mixtures enhanced soil C-hydrolase and C-oxidase activities.

• The C-hydrolase activities increased with plant functional type richness.

• The C-oxidase activities decreased with plant species richness.

• Soil organic C (SOC) and microbial biomass C increased with C-hydrolase.

• Species richness differentially affected C-degrading enzymes and SOC storage.

Abstract

Microbial decomposition of soil organic carbon (SOC) is a major determinant of the global climate and terrestrial ecosystem services. Despite the rapid loss of plant species worldwide, it remains unclear how plant species richness impacts SOC decomposition, especially the decomposition of labile vs. recalcitrant SOC. This is partly because of the variable responses of soil C-degrading enzyme activities to plant species richness. Through a global meta-analysis of 490 paired observations of plant mixtures versus monocultures, we show that plant mixtures significantly enhanced soil C-hydrolase (degrades labile C) and C-oxidase (degrades recalcitrant C) activities by 29.4 and 14.9%, respectively. However, in mixtures, C-hydrolase activity marginally (P = 0.051) increased, while C-oxidase activity significantly decreased with plant species richness. In addition, in mixtures, C-hydrolase but not C-oxidase activity significantly increased with plant functional type richness and experimental duration. These plant species richness and functional type effects on C-hydrolase and C-oxidase activities were consistent among diverse terrestrial ecosystems, plant life forms, the presence/absence of legumes, and climate types. Moreover, increases in C-hydrolase but not C-oxidase activity were positively related with increasing microbial biomass C and SOC under plant mixtures, suggesting that faster microbial decomposition and transformation of labile C pools mediate SOC accumulation at higher plant species richness. These results highlight that plant species richness differentially affects labile and recalcitrant C-degrading enzymes, thereby influencing SOC decomposition, dynamics, and accumulation.

Introduction

Plant species diversity is declining at an alarming rate as a complex response to human-induced global changes (Tilman and Lehman, 2001; Newbold et al., 2015). Such ecological changes have prompted extensive research to understand the impact of plant species loss on ecosystem functions and services (Handa et al., 2014; Chen et al., 2018b; Hautier et al., 2018; Huang et al., 2018). Soil organic C (SOC) represents the largest C reservoir in terrestrial ecosystems. The decomposition of SOC plays vital roles in regulating the climate and maintaining the soil's ecological functions (Jackson, 2000; Lal, 2004). Recent studies have revealed positive impacts of plant species richness on SOC content and stock (Lange et al., 2015; Chen et al., 2018b), and soil microbial biomass and respiration (Fig. 1) (Khlifa et al., 2017; Prommer et al., 2020). However, it remains unclear how plant species richness impacts microbial decomposition of SOC and whether these impacts are linked to soil microbial C (MBC), microbial respiration and SOC storage (Fig. 1). This is partly due to the lack of understanding of how plant species richness impacts soil extracellular enzyme activities (EEAs), the proximate index of SOC decomposition (Burns et al., 2013).

Soil organic C is incredibly complex, and separating it into fractions that have different behaviors is crucial for mechanistic understanding the complex responses of SOC to global change (Lehmann and Kleber, 2015; Christopher et al., 2018). Soil organic C is often categorized into labile and recalcitrant C fractions in terms of their susceptibility to decomposition (Davidson and Janssens, 2006; Cotrufo et al., 2013). Soil labile C compounds, such as cellulose, hemicellulose and simple root exudates, can be degraded by C-hydrolases, such as β-1,4-glucosidase, β-1,4-xylosidase, β-D-cellobiosidase, cellulase and invertase (Jian et al., 2016; Chen et al., 2018a). Recalcitrant C compounds, such as lignin, phenolic and other large aromatic C compounds, can be oxidized and degraded by C-oxidases, including peroxidase, phenol oxidase, and polyphenol oxidase (Burns et al., 2013; Chen et al., 2018a). Synthesis and secretion of these C-degrading enzymes are largely dependent on soil substrate availability and quality (Sinsabaugh et al., 2008; Burns et al., 2013), which are affected by plant species richness in an ecosystem.

Plant species richness has been widely found to promote plant productivity through complementary resource utilization among species or through selection effects of the most productive species (Reich et al., 2012; Huang et al., 2018). Increased plant productivity can facilitate both labile and recalcitrant C input via plant shoot and root litter production and release of root exudates (Fig. 1) (Lange et al., 2015; Ma and Chen, 2018; Zheng et al., 2019), thereby increasing substrate availability and the activities of C-hydrolases and C-oxidases. Nevertheless, empirical studies have showed positive (Lucas-Borja et al., 2012; Ma et al., 2017), neutral (Cong and Eriksen, 2018) and negative (Tian et al., 2013; Mu et al., 2019) effects of increased plant species richness on both C-hydrolases and C-oxidases activities. These divergent effects may be caused by differences in plant species richness, plant functional type (e.g., grasses, herbs and legumes), experimental duration, ecosystem type and climate region across studies. A synthesis of studies that manipulate plant species richness might help elucidate the mechanisms underlay these divergent effects, and determine the global effects of plant species richness on SOC-degrading EEAs. In addition, soil C-degrading enzymes produce substrates for microbial anabolism and respiration (Burns et al., 2013; Liang et al., 2017). Changes in SOC-degrading EEAs are thus expected to be linked with increased microbial respiration, and MBC and SOC content under higher plant species richness (Chen et al., 2019a, 2019b), yet direct evidence is lacking (Fig. 1). Determining the associations between changes in C-related variables and SOC-degrading EEAs will improve our understanding of plant species richness effects on SOC dynamics.

We conducted a global meta-analysis using 490 paired observations of plant mixtures (multiple plant species) and monocultures (single plant species) from 76 studies to investigate the responses of C-hydrolase and C-oxidase activities to plant species richness and their links with the responses of microbial respiration, MBC, and SOC. We first evaluated the overall effect of plant mixtures on soil C-hydrolase and C-oxidase activities. We then tested whether these effects would increase with plant species richness and functional type richness in mixtures, and with experimental duration. We also tested whether these effects would change among different ecosystem types, plant life forms, the presence/absence of legumes, and across different climates. Finally, we examined whether the responses of soil C-hydrolase and C-oxidase activities to plant mixtures were linked with changes in microbial respiration, MBC and SOC. This research will help reconcile some of the discrepancies in our understanding of plant species richness effects on SOC in diverse ecosystems.