Patterns and determinants of soil microbial residues from tropical to boreal forests

Highlights

• Microbial residue concentrations increased significantly from tropical to boreal forests soils.

• Pattern of microbial residues was mainly driven by temperature and soil N.

• Fungal residues preferentially accumulated in high latitude relative to bacterial residues.

• Contribution of microbial residues to SOC decreased from tropical to boreal forests.

Abstract

Soil carbon (C) stabilization has become an important topic in recent years in the context of global climate change. Increasing evidence suggests that microbial residues represent a significant fraction of persistent soil C pools. However, patterns and determinants of soil microbial residues across different biomes remain poorly understood. Here, by combining field investigations from tropical to boreal forests in eastern China with a meta-analysis across global forest biomes, we assessed how biotic and abiotic factors governed the geographic pattern of soil microbial residues indicated by amino sugars. We found that microbial residue concentrations in soils increased significantly from tropical to boreal forests in China and across the globe, which was mainly driven by temperature and soil nitrogen (N). Compared with bacterial residues, fungal residues preferentially accumulated at high latitudes. However, a significant negative relationship existed between soil C/N ratio and total residue-C/SOC in all examined forest soils, indicating a greater contribution of microbial residue-C to SOC in tropical forests than in boreal forests. These findings demonstrate that climate and soil play an important role in microbial-mediated soil C stabilization from boreal to tropical forests.

Introduction

Interest in the transformation and sequestration of soil organic carbon (SOC) has increased significantly in recent years because of the importance of SOC in the global carbon (C) cycle (Schmidt et al., 2011; Lehmann and Kleber, 2015; Crowther et al., 2019). Dynamics of soil C pools in terrestrial ecosystems are heavily influenced by microbial catabolism and anabolism (Schmidt et al., 2015; Liang et al., 2017). Microbial contributions to soil C sequestration have been historically regarded as marginal or even negligible because microbial biomass has a fast turnover rate and only accounts for a small fraction of SOC (<4%) (Anderson and Joergensen, 1997). However, increasing evidence shows that microbial catabolic and anabolic processes play a central role in regulating the sequestration of stable C in soils (Simpson et al., 2007; Liang et al., 2011, 2019; Miltner et al., 2012; Ma et al., 2018). Soil microbes convert plant C into microbial cellular components and byproducts during the decomposition of plant debris. Microbial necromass (intact cell or after lysis and fragmentation) can be selectively preserved in soils by being adsorbed onto mineral surfaces, incorporated into organo-mineral complexes or occluded within inaccessible pore spaces at the submicron scale (Liang et al., 2017, 2019). For instance, soil microbial necromass contributes approximately 30–60% on average to SOC in temperate arable lands, grasslands and forests (Liang et al., 2019). However, it remains poorly understood how climate, soil and plants interact and drive microbial residue accumulation and its contribution to SOC in forest ecosystems. Exploring the geographical pattern of microbial residue accumulation and its related mechanisms is urgent for understanding the formation and stability of soil C in forest ecosystems.

The accumulation of soil microbial residues is regulated by biotic and abiotic factors. A complex relationship exists between living microbial biomass and their residues because microorganisms produce residues through synthetic metabolites and decompose microbial residues at the same time (Liang et al., 2017; Ma et al., 2020). Meanwhile, abiotic factors affect microbial residues by regulating microbial metabolites. Soil N availability plays an important role in both microbial growth and its byproduct formation (Cotrufo et al., 2013). For instance, elevated N inputs facilitate the formation of new fungal residues but retard the deposition of old residues in a temperate forest (Griepentrog et al., 2014). The change of litter quality (indicated by carbon/nitrogen ratio) resulted from shifts in vegetation composition could affect the efficiency of production of microbial residues as well (Jolivet et al., 2006; Zhang et al., 2013; Schmidt et al., 2015; Shao et al., 2019). Moreover, soil texture could determine the persistence of microbial residues in soil matrix (Chantigny et al., 1997; Zhang et al., 1998; Six et al., 2006; Ni et al., 2020). However, the effect of soil texture on microbial residue accumulation depends on the climate (Ma et al., 2018). In the coarse-textured soils, microbial residue accumulation decreases with increasing climate aridity (Ma et al., 2018).

Because temperature and precipitation regulate soil weathering, vegetation composition and microbial activity, the accumulation of soil microbial residues may vary widely in different forest biomes. Tropical forests have a low level of SOC due to a fast turnover under high temperature and precipitation, while boreal forests have a high level of SOC due to a long residence time under low temperature (Carvalhais et al., 2014). However, most microbial residues are mineral associated organic C, which is often greater in soils with higher microbial activity and higher clay content (Cotrufo et al., 2013; Crowther et al., 2019). Therefore, the contribution of microbial residues to SOC may be greater in warmer and wetter ecosystems, as high temperature and precipitation should increase microbial activity and promote soil weathering. Indeed, recent studies showed that the contribution of microbial residues to SOC was higher in tropical forests (Zhang et al., 2016; Ma et al., 2020) than in temperate forests (Khan et al., 2016; Liang et al., 2019). These results suggest that the accumulation of microbial residues and its contribution to SOC may vary largely among different forests of various climates.

To explore the geographical patterns and controlling factors of soil microbial residues in different forest biomes, we conducted a field survey on the concentrations of soil amino sugars from tropical to boreal forests in eastern China, and quantified the relative importance of environmental variables, such as climate, soil and plant factors, in shaping these patterns. To cover possible risk caused by the small number of survey sites in our study, we further collected data of soil microbial residues reported across the world's forests and performed a meta-analysis for a range of forest biomes. In this study, we hypothesized that, (1) the concentrations of microbial residues in soils would increase from tropical to boreal forests, because warm climates in low latitudes can result in the rapid turnover of soil organic matter and limit the accumulation of microbial residues in soils compared to high latitudes, and (2) the proportion of microbially-derived C in SOC would decrease from tropical to boreal forests, because the activity of soil microorganisms is limited by the cold climate in boreal forests and soil organic matter is highly processed in tropical forests.