Elsevier

Applied Soil Ecology

Volume 155, November 2020, 103664
Applied Soil Ecology

Soil texture and straw type modulate the chemical structure of residues during four-year decomposition by regulating bacterial and fungal communities

https://doi.org/10.1016/j.apsoil.2020.103664Get rights and content

Highlights

  • Straw residues and associated microbiome was studied in a four-year experiment.

  • In sand soil the texture drive convergence of microbiome and litter chemistry.

  • In clay and loam soil the straw drive divergence of microbiome and litter chemistry.

  • Chemical change of straw is depended on drivers structuring decomposer communities.

Abstract

The changes of chemical structure and decomposer community during straw degradation have been inconsistent in previous reports, showing either convergence or divergence of chemical structures or microbial communities among different straw types. Hence the strength of their relationship remains unclear. Here, we directly measured the chemical structures and bacterial and fungal communities of wheat (Triticum aestivum L.) and maize (Zea mays L.) residues after four-year decomposition in three Calcaric Fluvisols that varied in soil textures. Separation of the chemical structures among the six soil-straw combinations (two straw types × three soil textures) were generally coupled with trends in the communities of bacterial and fungal decomposers, but the nature of their coupling differed. In the sand soil, soil texture was the central feature that shaped bacterial and fungal communities for both straw types, driving in turn the convergence of chemical structures of both decomposing straws. In contrast, in the sandy loam and silty clay soils, straw type was the primary regulator of the colonizing bacterial and fungal communities, which resulted in the divergence of chemical structures according to straw type.

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)

  • S.D. Siciliano et al.

    Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities

    Soil Biol. Biochem.

    (2014)
  • M.D. Wallenstein et al.

    Litter chemistry changes more rapidly when decomposed at home but converges during decomposition-transformation

    Soil Biol. Biochem.

    (2013)
  • M. Xia et al.

    Soil quality in relation to agricultural production in the North China Plain

    Pedosphere

    (2015)
  • W. Zech et al.

    Factors controlling humification and mineralization of soil organic matter in the tropics

    Geoderma

    (1997)
  • F. Abbasian et al.

    Microbial diversity and hydrocarbon degrading gene capacity of a crude oil field soil as determined by metagenomics analysis

    Biotechnol. Prog.

    (2016)
  • M.K. Aneja et al.

    Microbial colonization of beech and spruce litter—influence of decomposition site and plant litter species on the diversity of microbial community

    Microb. Ecol.

    (2006)
  • B.J. Baker et al.

    Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria

    Microbiome

    (2015)
  • R.A. Batista-García et al.

    Characterization of lignocellulolytic activities from fungi isolated from the deep-sea sponge Stelletta normani

    PLoS One

    (2017)
  • B. Berg et al.

    Plant Litter Decomposition, Humus Formation, Carbon Sequestration

    (2008)
  • B. Blasi et al.

    Pathogenic yet environmentally friendly? Black fungal candidates for bioremediation of pollutants

    Geomicrobiol J.

    (2016)
  • G. Bonanomi et al.

    Comparing chemistry and bioactivity of burned vs. decomposed plant litter: different pathways but same result?

    Ecology

    (2018)
  • X. Cao et al.

    Solid-state NMR analysis of soil organic matter fractions from integrated physical-chemical extraction

    Soil Sci. Soc. Am. J.

    (2011)
  • J.G. Caporaso et al.

    QIIME allows analysis of high-throughput community sequencing data

    Nat. Methods

    (2010)
  • H. Chen et al.

    Application of high-throughput sequencing in understanding human oral microbiome related with health and disease

    Front. Microbiol.

    (2014)
  • K.R. Clarke

    Non-parametric multivariate analyses of changes in community structure

    Aust. J. E.

    (1993)
  • T.Z. DeSantis et al.

    Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB

    Appl. Environ. Microbiol.

    (2006)
  • O. Dilly et al.

    Bacterial diversity in agricultural soils during litter decomposition

    Appl. Environ. Microb.

    (2004)
  • P. Dixon

    VEGAN, a package of R functions for community ecology

    J. Veg. Sci.

    (2003)
  • R.C. Edgar

    Search and clustering orders of magnitude faster than BLAST

    Bioinformatics

    (2010)
  • FAO

    World Reference Base for Soil Resources. World Soil Resources. Report 84

    (1998)
  • N. Fierer et al.

    Toward an ecological classification of soil bacteria

    Ecology

    (2007)
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