Efficient decomposition of lignocellulose and improved composting performances driven by thermally activated persulfate based on metagenomics analysis

https://doi.org/10.1016/j.scitotenv.2021.148530Get rights and content

Highlights

  • Self-generating heat during composting could activate persulfate to produce SO4·.

  • SO4· could accelerate the degradation of lignocellulose.

  • Actinobacteria and Proteobacteria were vital for lignocellulosic degradation.

  • GHs and AAs gene abundances were higher in PS than in CK by metagenomics analysis.

Abstract

In this study, fresh dairy manure and bagasse pith were used as raw materials to study the effect of potassium persulfate in the aerobic composting process. The influence of sulfate radical anion (SO4·) generated by thermally activated persulfate on physicochemical parameters, lignocellulose degradation, humic substance (HS) formation, microbial community succession, and carbohydrate-active enzymes (CAZymes) composition were assessed during composting. Experimental results showed that the degradation rates of cellulose, hemicellulose and lignin in the treatment group with potassium persulfate (PS) (61.47%, 74.63%, 73.1%) were higher than that in blank control group (CK) (59.98%, 71.47%, 70.89%), respectively. Additionally, persulfate additive promoted dynamic variation of dissolved organic matter (DOM) and accelerated the formation of HS. Furthermore, metagenomics analysis revealed that persulfate changed the structure of the microbial community, and the relative abundances of Actinobacteria and Proteobacteria increased by 17.64% and 34.09% in PS, whereas 12.09% and 29.96% in CK. Glycoside hydrolases (GHs) and auxiliary activities (AAs) families were crucial to degrade lignocellulose, and their abundances were more in PS. Redundancy analysis (RDA) manifested that Actinobacteria and Proteobacteria were closely associated with lignocellulosic degradation. In brief, persulfate could accelerate the degradation of organic components, promote the formation of HS, optimize the structure of microbial community, and improve the compost quality.

Introduction

With the continuous improvement of public quality and environmental awareness, how to deal with organic agricultural wastes had aroused people's extensive attention (Jiang et al., 2020a). Compared with incineration and landfill, composting is a better method to dispose organic agricultural solid wastes (Wei et al., 2014). It is a physiological and biochemical process dominated by microorganisms, which can kill pathogens through high-temperature to make the compost harmless and transform the organic solid wastes into humus-rich organic fertilizer (Zhu et al., 2020).

The recalcitrance of lignocellulose with special structure(cellulose and hemicellulose are closely wrapped by polymerized lignin), results in an inferior biodegradation efficiency and long-periodic reaction during the degradation of organic agricultural solid wastes (Sawatdeenarunat et al., 2015; Huang et al., 2019; Den et al., 2018; Wu et al., 2020). As a part of sustainable development materials, how to accelerate the degradation and reinforce the utilization of lignocellulose are great significance (Jurado et al., 2015). The study from Sun and Cheng (2002) showed lignocellulose was a prospectively alternative production of chemicals and fuels, and produced more sugar for fermentation into ethanol by increasing the efficiency of cellulose hydrolysis. In addition, the combined application Fenton pretreatment and composting significantly increased the lignocellulose-degradation enzymes activities (Wu et al., 2019). The effect of adding non-ionic surfactant on the degradation of lignocellulose and the formation of humic substance (HS) were investigated by Li et al. (2020). Moreover, in the process of anaerobic fermentation, magnetic nanoparticles could accelerate the degradation of organic matter (OM) through electron transfer (Zhou et al., 2021). Besides, lots of researchers are looking for more suitable methods or additives to accelerate the biodegradation of recalcitrant organic components during composting.

Persulfate was widely used to effectively remove organic pollutants such as diclofenac, atrazine, 2,4-dichlorophenoxyacetic acid, phenol and extracellular polymeric substances (Chen et al., 2016; Lin et al., 2011; S.H. Wu et al., 2018; Ruan et al., 2021). Furthermore, sulfite removing the pollutants in water treatment was also studied (Wu et al., 2021). Commonly, persulfate could be activated by heat, base, ultraviolet light, microwave, corn biochar, ultrasound and transition metals to produce sulfate radical anion (SO4·) (Anipsitakis et al., 2006; Wang and Wang, 2018; Bian et al., 2021). Among these activation methods, thermal activation (>50 °C) was a high-efficiency activation method via destroying oxygen peroxide bond (Liu et al., 2017; Cai et al., 2018). Furthermore, SO4· is an electrophilic reagent and it reacts with organic compounds by electron transfer, thus removing organic pollutants (Wojnárovits and Takács, 2019; Deng et al., 2013). Especially, SO4· can not only remove total organic carbon in a broad range of pH, but also break the structure of lignocellulose (Zhu et al., 2018; Loow et al., 2017). We speculate if persulfate is introduced into composting process, under the condition of composting temperature reach above 50 °C for more than 7 days during thermophilic period, the self-generated heat during composting can activate persulfate to generate SO4·, which will benefit to enhance lignocellulosic degradation efficiency in composting. It is mainly because SO4· is prone to react with phenolic radicals, hydroxyl, or alkoxy electron-donating groups of lignin structure (Fagier et al., 2016). Thereby, SO4· can accelerate the exposure of cellulose and hemicellulose by decomposing lignin structure, and the accessibility of cellulose molecules and complex enzymes will be improved to achieve a better synergistic degradation of lignocellulose.

Investigating related microorganisms and their secreted enzymes is a great significance to further understand the synergistic degradation relationship among cellulose, hemicellulose and lignin during composting. Nevertheless, the traditional microbial research method was limited understanding microorganisms and enzymes during lignocellulosic degradation, due to only 1–3% of the microbial information was understood (Rubin Edward, 2008). Therefore, a new research approach is needed to overcome the drawback of further understanding the information of microorganisms and enzymes. Metagenomics (a new generation of sequencing technology for obtaining all the genetic information in microbial community) was used as to study the genes related to lignocellulose degradation, which could establish a comprehensive information system about the composition of microbial communities during composting (Awasthi et al., 2020). Ma et al. (2020) analyzed the gene expression of carbohydrate active enzymes (CAZymes) related to depolymerize lignocellulose in a synergistic manner by metagenomics. Hence, in this work, metagenomics was used to analyze the microbial community succession and enzyme family composition in composting, to explore the relationship between environmental factors and microorganisms, and to study the environmental conditions of microbial secretory enzymes, such as glycoside hydrolases (GHs) and auxiliary activities (AAs).

The detailed objectives of this study were: (I) to detect the influence of potassium persulfate on physicochemical parameters (temperature, pH, moisture, OM) and the degradation of lignocellulose; (II) to evaluate the effect of potassium persulfate addition on dissolved organic matter (DOM) and HS dynamics; (III) to investigate the significance of CAZymes families and the carbon metabolism by metagenomics; (IV) to analyze the relationship between environmental factors and pivotal phyla. This study will provide a theoretical basis for seeking a novel approach, to promote the degradation and conversion of recalcitrant lignocellulose during composting.

Section snippets

Composting experiment design and sampling

In this study, fresh dairy manure and bagasse pith were evenly mixed with a wet weight ratio of 4:1 for a total weight of per compost pile of 20 kg, which guaranteed the compost initial moisture rate was about 65%. Additionally, the study included two treatments: a control (CK) and a test group with 0.5% (w:w, dry weight) potassium persulfate (PS). Fresh dairy manure and bagasse pith were obtained from Guangxi University and Nanxu Sugar Factory (Nanning, China), respectively. Potassium

Analysis of physicochemical parameters during composting

Physicochemical parameters (temperature, moisture, pH, OM) were vital for judging performances and maturity during composting, as shown in Fig. 1. Temperature is the basic index to evaluate the degree of composting, which is the direct manifestation of the mini-succession of microbial community and degradation of OM (Zhu et al., 2021), Fig. 1(a). The temperatures in CK and PS were rapidly reached 64 °C and 66 °C within 24 h entered thermophilic phase (>50 °C), and the temperature of PS group

Conclusion

The persulfate was activated by composting thermophilic phase (>50 °C) to produce SO4·, which promoted the degradation of lignocellulose, improved the transformation of DOM, accelerated the formation of HS in composting process. About 3% more degradation rate of lignocellulose and about 6% more content of HS were observed in PS than in CK. Additionally, the variation of environmental factors affected the microbial community succession during composting, Actinobacteria and Proteobacteria were

CRediT authorship contribution statement

Susu Wang: Data curation, Methodology, Investigation, Formal analysis, Writing-original draft. Qingran Meng: Methodology, Investigation. Qiuhui Zhu: Investigation, Software. Qiuqi Niu: Investigation. Hailong Yan: Data curation. Kecheng Li: Data curation, Investigation. Gen Li: Methodology, Investigation. Xintian Li: Data curation, Investigation. Haibo Liu: Writing-review & editing. Youyan Liu: Writing-review & editing. Qunliang Li: Conceptualization, Supervision, Funding acquisition,

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

The authors are thankful to the National Natural Science Foundation of China (No. 21878057) and the Natural Science Foundational of Guangxi (No. 2017GXNSFAA198345) for financial supports.

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