Patterns of fungal community succession triggered by C/N ratios during composting

https://doi.org/10.1016/j.jhazmat.2020.123344Get rights and content

Highlights

  • Composting treatment and phase influenced fungal community.

  • Composting reduced plant and animal pathogens.

  • Plant and animal pathogens were negative correlated with compost maturity.

  • Specific OTUs were expected to compete for environmental preferences (niches).

Abstract

Accumulating evidence indicates that the functional rather than taxonomic composition of microbial communities is closely correlated to local environmental factors. While composting is a widely accepted practice, specific knowledge of how fungal functional groups interact during the composting process remains limited. To address this, the impact of the initial C/N ratio of composting material on fungal community was analyzed in order to reveal the succession of functional diversity. Compared with the raw materials, the final composting product significantly reduced the relative abundances of plant and animal pathogens. Abundances of plant and animal pathogens, as well as dung saprotrophs, were negatively correlated with compost maturity, while abundances of wood saprotrophs exhibited positive correlations. Specific OTUs that showing highly abundant in each treatment were expected to compete for environmental preferences (niches) and/or interact with each other in positive (facilitative) ways. OTU2 (wood saprotroph) exhibiting the highest occurrence was negatively related to OTU7 (animal pathogen) and OTU4 (plant pathogen) during the mesophilic phase. Taken together, high-efficiency composting is represented as pattern variations of fungal community with a process of gradual decline of plant and animal pathogens as well as dung saprotrophs.

Introduction

Intensive animal husbandry results in large-scale production of livestock and poultry manure which imposes environmental challenges. The widespread utilization of manure as a resource for enhancing plant productivity can serve to reduce environmental impacts (Ma et al., 2018). Composting imparts benefits to a soil such as through the reduction or elimination of pathogens and weed seeds, supporting the formation of humus and reducing relatively persistent organic compounds (Li et al., 2015; Ye et al., 2019a; Ye et al., 2019b). The composting process is influenced by physico-chemical parameters such as temperature, C/N ratio, oxygen availability and the degree of compaction (Onwosi et al., 2017). Among these, the C/N ratio is the most critical factor that influences composting efficiency (Huang et al., 2004). Efficient composting can be influenced by modifying the C/N ratio through the addition of carbon-rich bulking agents (Zhou et al., 2014). As C and N are key microbial metabolic nutrients (Iqbal et al., 2015), elucidating the chemical and biological changes that occur during the composting process triggered with different initial C/N ratio can aid in the optimization of the quality of composting product.

From a microbiological perspective, composting is an exceptionally complex process in which microbial activity plays pivotal role in biotransformation of organic substrates. Most research has focused solely on the compost bacterial community (Tortosa et al., 2016; Storey et al., 2015) while neglecting the role of the fungal community that degrade organic residues such as cellulose and lignin (Ryckeboer, 2003). Owing to the variable environmental conditions, fungal communities have demonstrated succession during the composting process (mesophilic, thermophilic and mature phases) due to distinct roles in the degradation of organic matter to stable and mature humic substance thus contribute to composting maturity (Gannes et al., 2013; Belyaeva and Haynes, 2009), which refers to the degree of decomposition of phytotoxic compounds and the absence of plant or animal pathogens, leading to a stable and suitable product (Ryckeboer, 2003).

There is increasing evidence that the functional composition, rather than the taxonomic composition of the microbial community in natural environments is closely related to environmental properties (Louca et al., 2016; Nelson et al., 2016). That is, variations in metabolic functioning among organisms are thought to be a result of selection for specific metabolic pathways, based on external physicochemical conditions. This applies to alterations in the fungal community during the composting process as well, with metabolic functions that directly reflect the capacity for transformation and stabilization of organic material. Therefore, knowledge regarding the mechanisms that influence and organize the compost fungal community is essential for effective compost management. To this end, while fungal taxonomic succession through the composting process has been well documented (Xi et al., 2014), there remains a limited understanding concerning the functional roles of the fungal community due to highly diverse guilds and the lack of ecologically meaningful categories. To attempt to address this, FUNGuild, a tool that can be used to taxonomically parse fungal sequences by ecological guild independent of sequencing platform or analysis pipeline (Nguyen et al., 2016), was developed to predict the functional diversity of the fungal community. This bioinformatic tool has been applied to analyze fungal trophic structure in soil (Toju et al., 2016) and compost (Wang et al., 2018a,b) while interactions among fungi with different primary trophic strategies during the composting process has received less attention. A thorough understanding and characterization of fungal community functional succession during composting may lead to improvements in terms of process reproducibility, performance and the quality of the finished product.

In our previous research, compost C/N ratios were adjusted through the application of varying amounts of sawdust into cow manure and mushroom residue in order to elucidate how specific bacterial species were correlated to high-efficiency composting (Qiao et al., 2019). In the present study, targeted MiSeq sequencing combined with FUNGuild was used to perform an in-depth assessment concerning the functional patterns of fungal community succession during composting. Overall, the research objectives were: 1) to determine the effect of varying C/N ratios on the functional fungal succession and community composition; (2) to elucidate the relationship between principle functional groups and compost maturity; (3) to infer how functionally diverse fungi are compartmentalized into networks of potential interactions according to composting phase.

Section snippets

Compost materials and experimental design

Thermophilic aerobic composting was conducted that was composed of cow manure, sawdust, and mushroom residue as the raw materials in Huaian, China (33°36′ N, 119°01′ E). Three windrows were implemented with three different C/N ratios of 15 (pile 1), 25 (pile 2) and 35 (pile 3) (Table 1). Samples were collected at the mesophilic (days 0 and 1), thermophilic (days 5 and 16), and mature phases (days 25 and 39) at five locations of seven sections to ensure the representativeness, and then mixed to

Variations of diversity of fungal community

After quality control, a total of 5,163,649 ITS sequences (mean = 40,981 per sample) clustered into 3,522 OTUs were obtained for all composting samples. Estimates of fungal α-diversity were based on evenly rarefied OTU matrices (14,546 sequences per sample) at compost developmental time points in each treatment. Consistent richness with increases in diversity until day 5 were observed, followed by a decreasing tendency in both measures with time, indicating the impacts of the thermophilic and

Conclusion

This study provides the high-resolution assessment of fungal functional group patterns during composting across C/N ratios. Plant and animal pathogens exhibited significantly negative relationships while wood saprotrophs were positively correlated with compost maturity. Simultaneously, wood saprotrophs were negatively correlated to dung saprotrophs, as well as plant and animal pathogens, indicating that thermophilic aerobic composting is a process of gradual decrease in plant and animal

Declaration of Competing Interest

The authors declare no conflict of interest.

Acknowledgements

This research was supported by the National key research and development program (2018YFD0500201), the Agricultural Science and Technology independent innovation fund project of Jiangsu Province (CX(19)2026), the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD), the 111 project (B12009), and the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56).

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