Can biochar and oxalic acid alleviate the toxicity stress caused by polycyclic aromatic hydrocarbons in soil microbial communities?

Highlights

• Contaminants stress shifted microbial community structures in soil.

• Biochar and OA mediated the shifts of soil microbial communities stressed by PAH.

• Biochar and OA stimulated the functional genes participating in PAH degradation.

• Tandem biochar-rhizoremediation may be feasible to improve PAH-polluted soil.

Abstract

It remains unclear whether biochar amendment can mediate changes in soil microbial communities caused by organic contaminants in the rhizosphere. In this study, phenanthrene-contaminated soil was amended with biochar and oxalic acid (OA) alone or in combination and incubated for 21 days. Phospholipid fatty acids (PLFAs) and high-throughput sequencing were used to evaluate shifts in bacterial and fungal community structure. Phenanthrene stress led to significant shifts in both soil bacterial and fungal community structure, in particularly, 82% of microbial phyla decreased in abundance. Biochar and/or OA improved the phenanthrene-polluted soil by positively mediating shifts in soil microbial communities stressed by phenanthrene. Specifically, biochar and/or OA led to the survival of certain microbial taxa that were inhibited by phenanthrene stress. In addition, many functional microbial individuals and genes participating in polycyclic aromatic hydrocarbon (PAH) degradation were positively stimulated by high phenanthrene stress and further stimulated by the simultaneous application of biochar and OA. Based on these findings, tandem biochar and rhizoremediation may be a feasible strategy for relieving PAH toxicity to soil microbial communities.

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are among the most widespread and persistent organic contaminants and have attracted increasing attention due to their ecotoxic, carcinogenic, and mutagenic properties (Joner et al., 2011). PAHs are toxic not only to humans through food chains or air exposure but also to the soil biota (e.g., microorganisms) (Gupta et al., 2015). PAHs affect microbial diversity (Liu et al., 2017) and function (Chaudhary et al., 2012) and thus the ecological behaviors, such as carbon and nutrient cycling and energy metabolism, of soil microbial communities (Sverdrup et al., 2002; Anyanwu and Semple, 2016). However, a diverse soil microbial community is essential for soil ecological stability because soil microbes are the main drivers of the biogeochemical cycles of nutrients and elements in soil (Ren et al., 2018). Microbial communities can also contribute to the effective degradation of PAHs in soil (Joner et al., 2011), therefore, insights into the changes in microbial community structure under PAH stress are critical.

Biochar, a carbon-rich material, is regarded as an effective amendment for reducing environmental threats posed by contaminants in soil (Wang et al., 2012). PAHs can be immobilized by biochar in soil, decreasing their bioavailability and transport (Song et al., 2017). In addition, due to the nutrient properties (Sohi et al., 2010) and porous structure of biochar (Quilliam et al., 2013), its addition to soil can facilitate the growth of soil microbes. Biostimulation by biochar leads to increased dissipation of PAHs in contaminated soil (Kong et al., 2018). Moreover, soil improvement, such as increasing soil aggregation, soil water and nutrient retention and soil pH, has also increased the popularity of biochar (Muhammad et al., 2018; Zheng et al., 2018). In healthy soil, a rich and balanced microbial community structure is indispensable. However, whether biochar addition to PAH-polluted soil can improve the responses of soil microbial community structure to toxicity stress from PAHs and thus improve the polluted soil is unknown.

Biochar has generally been applied to agricultural fields for soil improvement (Hammond et al., 2011), therefore, it comes into contacting with the primary location of microorganisms in agricultural soil, the rhizosphere (Rohrbacher and St-Arnaud, 2016; Blagodatskaya et al., 2014). In rhizosphere soil, root exudates, such as low-molecular-weight organic acids (LMWOAs), can be used as labile carbon resources for microbial growth (Thomas and Cébron, 2016), leading to simultaneous increases in microbial biomass and activity. At the same time, the bioavailability of contaminants can be enhanced by facilitating their release from soil or even biochar (White et al., 2003; Song et al., 2016), leading to enhanced contaminant biotoxicity. Cébron et al. (2011) found that root exudates favored the increase of bacterial community diversity in PAH-contaminated soil. Guo et al. (2017) observed increased dissipation of PAHs in soil with root exudates addition, which was due to increased bacterial abundance and diversity and positive stimulation of functional genes. The alleviation of contaminant phytotoxicity by root exudates has also been reported. The release of root exudates can modulate microbial community structure in the rhizosphere, and the enrichment of some functional degraders helps reduce the hazards of contaminants (Yang et al., 2007). In addition, in a contamination stressed soil environment, the release of root exudates can regulate the properties of rhizosphere soil, such as pH and oxidation-reduction properties, and thus affect the morphology, metabolism and transformation of contaminants, in turn reducing their biological toxicity (Sung et al., 2004). How root exudates affect the responses of microbial communities to PAH toxicity stress in biochar-amended rhizosphere soil is unknown and needs to be further studied.

The objective of this study was to elucidate whether biochar and root exudates affect the response of whole soil microbial communities to high PAH toxicity stress. Therefore, soils polluted with different levels of phenanthrene, one of the dominant components of PAHs in fields (Ma et al., 2015), were prepared and amended with biochar and root exudates individually or in combination. Oxalic acid (OA), a typical and dominant root exudate of ryegrass (Lolium multiflorum Lam) under PAH stress, was used to mimic the rhizosphere effect (Li et al., 2019). Phospholipid fatty acids (PLFAs) were analyzed to evaluate the shifts in soil microbial community structures. Furthermore, high-throughput sequencing was conducted to determine the responses of specific bacterial and fungal communities to phenanthrene stress and the mediation of this stress by biochar and/or OA. Finally, functional genes associated with PAH degradation were predicted based on the Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) algorithm and Kyoto Encyclopedia of Genes and Genomes (KEGG) database.