Impacts of red mud on lignin depolymerization and humic substance formation mediated by laccase-producing bacterial community during composting

Highlights

• The decomposition of organic matter was accelerated by adding red mud.

• Red mud promoted lignin degradation and HS formation during composting.

• Red mud additive affected the succession of laccase-producing microbial community.

• Proteobacteria was a crucial bacterial phylum secreting laccase.

• Temperature was a main factor driving the variation of microbial community.

Abstract

The aim of this study was to investigate the impacts of red mud on lignin degradation, humic substance formation and laccase-producing bacterial community in composting to better improve composting performances. The results indicated that the organic matter contents of final compost products in the treatment group with red mud (T) decreased by 25.74%, which was more than the control group without red mud (CK) (12.09%). The final lignin degradation ratio and humic substance concentration of the T were 18.67% and 22.80% higher than that of the CK, respectively. The final C/N values of compost in the CK and T were 11.32 and 10.66, respectively, which were both less than 15, suggesting that compost reached maturity. Redundancy analysis showed that temperature was the main factors driving the variation of laccase-producing bacterial community. Pearson analysis suggested that Pseudomonas, Phenylobacterium, and Caulobacter were the most significantly correlated with lignin degradation and humification in the T.

Introduction

In China, large amounts of livestock manures and agricultural wastes are produced every year, which cause serious environmental pollution (Wang et al., 2018, Wei et al., 2019). Composting, as an eco-friendly technology for treating these hazardous wastes, has received widespread attention (Xiao et al., 2019a, Li et al., 2019). During composting, microorganisms convert organic matter (lignin, cellulose, and hemicellulose) into stable humic substance (HS) as organic fertilizer for soil amendments (Li et al., 2019). The lignin-protein theory and phenol-protein theory, as the main theories of HS formation, show that lignin and its degradation products (phenols and quinones) are the key components of HS formation by polymerization with nitrogen-containing compounds (proteins and amino acids) (Guo et al., 2019, Tan, 2014). However, the degradation resistance of lignin hinders the decomposition of organic matter in the traditional aerobic composting (de Gonzalo et al., 2016, Wei et al., 2019), thereby reducing the formation of HS. Therefore, it is urgent to find a novel approach to enhance the degradation of lignin and the formation of HS during composting.

Lignin is a polyphenolic three-dimensional network-like aromatic compound composed of phenylpropanoid units connected by ether bonds and carbon-carbon bonds (Liu et al., 2020, Munk et al., 2015, Shi et al., 2020). Previous studies had confirmed that manganese peroxidase, lignin peroxidase and laccase were the three main enzymes to degrade lignin (Arora et al., 2002, Lopez et al., 2007, Wei et al., 2019). Compared with manganese peroxidase and lignin peroxidase, laccase uses oxygen as its electron acceptor to catalyze the oxidation of phenolic or non-phenolic lignin containing electrons (Munk et al., 2015). In addition, the catalyzed products of laccase do not contain harmful substances such as reactive oxygen species and H₂O₂, so it is called a green catalyst. Hence, more and more researchers pay attention to laccase in the field of composting. For instance, Lu et al. (2015) found that lignin degradation was closely related to the succession of laccase-encoding bacterial community in composting using the technology of PCR-Cloning. Chefetz et al. (1998) reported that laccase was involved in the process of humification during composting. Furthermore, it was claimed that laccase could oxidize phenols and generate free radicals which combine with proteins or amino acids to form HS during composting (Chefetz et al., 1998, Munk et al., 2015, Tan, 2014). These researches showed that laccase played the most important role in the depolymerization of lignin and the formation of HS during composting. However, studies pertinent to the investigation on improving laccase activity during composting have barely been reported. Thus, finding an inducer for promoting laccase activity is an effective way to accelerate the degradation of lignin and the formation of HS during composting.

Recently, additives have developed rapidly to improve the quality of compost, such as clay, zeolite, biochar, and red mud (Awasthi et al., 2019, Barthod et al., 2018, Wang et al., 2017). In particular, red mud as a hazardous waste from the alumina extraction industry also needs to be rationally managed. Red mud contains a large amount of iron-aluminum metal oxides with catalytic properties (Zhou et al., 2017), which has gradually attracted the interest of researchers focusing on composting. For instance, it was showed that red mud could significantly reduce the emissions of greenhouse gases (CO₂, CH₄, and NH₃) during composting (Barthod et al., 2018, Zhao et al., 2016). Additionally, red mud can affect the removal of antibiotic resistance genes and the succession of bacterial communities in swine manure composting (Wang et al., 2016). These researches successfully demonstrated the roles of red mud in composting. However, the effects of red mud on the lignin degradation and HS formation in composting have not been investigated. According to the previous studies, iron-aluminum metal oxides from red mud can absorb electrons from phenols and then turn into metal ion (Fe²⁺) (Hardie et al., 2009, Wu et al., 2018, Zhang et al., 2017). Among them, Fe²⁺ as the most important inducers of laccase, can increase the activity of laccase (Hermosilla et al., 2017, Salvachúa et al., 2013). Hence, it is speculated that red mud can be used as enzyme promoter to stimulate the laccase activity, thereby accelerating the lignin degradation and HS formation during composting.

All in all, the changes of physico-chemical parameters, the degradation of lignin, the formation of HS, and the succession of laccase-producing bacterial community were analyzed during composting. More importantly, the purpose of this research is to identify the effects of the introduction of red mud in composting on the relationship among lignin degradation, HS formation, and laccase-producing bacterial community, and to provide a new strategy for improving composting performances.