Soil texture and straw type modulate the chemical structure of residues during four-year decomposition by regulating bacterial and fungal communities
Introduction
The temporal changes in litter chemistry during decomposition have received increasing attention, but to date they have showed no consistent direction. Wickings et al. (2012) classified chemical pathways of litter decay into three patterns: (1) The “chemical convergence pattern”, by which initially divergent litter chemistries generally converged when 75–80% of the initial mass had been lost (Preston et al., 2009; Wang et al., 2012; Bonanomi et al., 2018); (2) The “the initial litter quality control pattern”, suggesting that initial differences in litter chemistry persisted throughout the decomposition process (Baumann et al., 2009; Li et al., 2015); and (3) The “decomposer control pattern”, by which the types of decomposer communities exerted dominant control on the chemical changes in the decomposing litters (Šnajdr et al., 2011; Wickings et al., 2011). Each chemical pathway would result in distinct chemical characteristics of persistent residues, which represent a major fraction of soil organic matter (SOM) (Kubartová et al., 2009) and contribute significantly to soil ecosystem functioning (Kögel-Knabner, 2002).
Litter decomposition is widely believed to be carried out by a consortium of microbes, and both the bacterial and fungal communities associated with decomposing litter undergo rapid successional changes so that different taxa dominate temporarily at different decomposition stages (Voříšková and Baldrian, 2013; Maarastawi et al., 2018). It is generally accepted that the dominance of r-strategists that utilize easily degradable compounds in early stages is eventually replaced by K-strategists, which degrade recalcitrant substrates, in later stages of decomposition (Fierer et al., 2007; Bastian et al., 2009). However, this general progression could potentially be altered by selective role of initial litter quality on their degrading microbes (Aneja et al., 2006; Baumann et al., 2009) or the distinct microbial taxa in different soils (Mula-Michel and Williams, 2013). In addition, assembly history—the competitive and facilitative interactions between early colonizers and new immigrants—governs the succession of decomposer community structure (Fukami et al., 2010). It is possible that small differences in early assembly history result in substantial differences in subsequent microbial composition, which would make microbial evolution unpredictable (Fukami et al., 2010). Therefore, further information is needed to clarify changes in the direction of decomposer community. Are they random or instead directionally constrained by ecological strategies of microbes, soil condition, or litter type?
Bonanomi et al. (2019) and Baumann et al. (2009) showed that chemical changes observed during decomposition interacted with shifts in microbial community composition. The replacement of r- by K-strategists during litter degradation could drive the convergence of chemical structure of residues to a recalcitrant nature (Berg and McClaugherty, 2008). However, other studies demonstrated that the regulatory effects of decomposer communities on chemical changes during litter decomposition were strongly influenced by initial litter type so that the imprints of initial chemistry persisted throughout the decomposition (Wickings et al., 2012; Wallenstein et al., 2013). Yet in other studies, changes in litter chemistry driven by decomposer communities also exhibited strong responses to specific soil conditions (Aneja et al., 2006; Wickings et al., 2011). This discrepancy may arise because simplistic broad categorization of microbial populations underestimates the divergent roles of decomposers having specific physiological capabilities (Wickings et al., 2011), so that changes in environmental factors (e.g. litter type or soil condition) could result in functionally different decomposer communities which could then modulate the chemical structure of residues. The relative importance of environmental factors in altering decomposer communities remains unclear.
The North China Plain (NCP) is a major agricultural production area in China, and has representative soil of Calcaric Fluvisol (FAO, 1998) with its texture ranging from sand to clay (Xia et al., 2015). Winter wheat and summer maize are widely grown in the NCP. Previous publications have shown that decomposer community composition could be altered by soil texture, probably through changing soil nutrition, moisture, and temperature conditions (Wickings et al., 2012; Mula-Michel and Williams, 2013).
In this study, we aimed to elucidate the specific directions of chemical and microbial changes of straw residues and their potential relationships, as influenced by straw type and soil textures. We directly assessed the chemical structures and microbial community compositions of residues persisting in the advanced decomposition stage at the NCP. Specifically, we buried wheat and maize straws in three Calcaric Fluvisol soils differing for their textures (sand, sandy loam, and silty clay), incubated for four years, and then detailed the chemical structures of the straws using solid-state 13C nuclear magnetic resonance (13C NMR) spectroscopy and residue-inhabiting microbial community compositions using 16S rRNA and ITS gene sequencing. The straw residues following four-year decomposition can be regarded as stable materials persisting after extensive decomposition, as we previously found that the straw masses decreased by 80% during an initial 10 months decomposition under conditions similar to those of the present study but decreased negligibly from 10 to 20 months (Li et al., 2020). We hypothesized that the chemical change of residues during degradation is depended on the dominant driver (straw type or soil textures) structuring decomposer communities.
Section snippets
Study site and litterbag experiment
A long-term field experiment located in Pandian, Fengqiu Country, Henan province, China (114° 34′ E, 35° 01′ N) was initiated in 1992 to investigate the effects of soil texture on crop performance. The most common soil in this area is classified as a Calcaric Fluvisol (FAO, 1998). Three Calcaric Fluvisol soils differing from one another by having textures of sand, sandy loam, and silty clay were collected in 1992 from the villages of Huangling (114° 42′ E, 34° 58′ N), Pandian (114° 34′ E, 35°
Weight losses of straw biomass, C, and N
Averaged across straw types and soil textures, 83.1%, 88.4%, and 95.6% of the original masses of straw biomass, C, and N respectively, were lost after four-year decomposition (Fig. 1). The ANOVA results further revealed that their losses were not significantly affected by straw type or soil texture (P > 0.05, Fig. 1).
Chemical structure
The chemical structures of the initial two straws were dominated by OCH, accounting for 49.9% of the total C in wheat and 46.2% in maize straw (Table 1; Fig. S1). The initial maize
Deviations of chemical structure in straw residues after four-year decomposition
Generally, the chemical changes in the decomposing straw residues were in accordance with the decay trajectory elaborated by many studies (Preston et al., 2009; Wang et al., 2012; Bonanomi et al., 2018), the loss of easily decomposable compounds, characterized by 13C NMR as O-alkyl and anomeric C, causing relative enrichment of more recalcitrant compounds such as aliphatic and aromatic materials. However, distinct differences in chemical composition, which were quantified by advanced
Conclusions
Our results emphasized a dominate role of residue-inhabiting microbial communities in shaping the chemical structure of straw residues. Yet both soil texture and straw type could regulate the bacterial and fungal communities harboured in the residue layer and thereby modulate the chemical structures. The relative importance of soil texture and straw type depended on the soil conditions during degradation. The chemically distinct compounds remaining after prolonged decomposition were considered
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.
Acknowledgements
This work was financially supported by the National Key Research and Development Program of China (2016YFD0300802), National Natural Science Foundation of China (41977102), and the China Agriculture Research System (CARS-03).
References (63)
- et al.
Impact of wheat straw decomposition on successional patterns of soil microbial community structure
Soil Biol. Biochem.
(2009) - et al.
Residue chemistry and microbial community structure during decomposition of eucalypt, wheat and vetch residues
Soil Biol. Biochem.
(2009) - et al.
Linking bacterial and eukaryotic microbiota to litter chemistry: combining next generation sequencing with 13C CPMAS NMR spectroscopy
Soil Biol. Biochem.
(2019) - et al.
Priming of soil organic matter: chemical structure of added compounds is more important than the energy content
Soil Biol. Biochem.
(2017) - et al.
Yucatán in black and red: linking edaphic analysis and pyrosequencing-based assessment of bacterial and fungal community structures in the two main kinds of soil of Yucatán State
Microbiol. Res.
(2016) - et al.
Carbon and nitrogen degradation on molecular scale of grass-derived pyrogenic organic material during 28 months of incubation in soil
Soil Biol. Biochem.
(2011) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter
Soil Biol. Biochem.
(2002)- et al.
Is there a convergence of deciduous leaf litter stoichiometry, biochemistry and microbial population during decay?
Geoderma
(2016) - et al.
Temporal dynamics and compartment specific rice straw degradation in bulk soil and the rhizosphere of maize
Soil Biol. Biochem.
(2018) - et al.
Assimilation of microbial and plant carbon by active prokaryotic and fungal populations in glacial forefields
Soil Biol. Biochem.
(2016)