Dynamic processes in conjunction with microbial response to disclose the biochar effect on pentachlorophenol degradation under both aerobic and anaerobic conditions

Highlights

• Biochar markedly inhibited PCP biodegradation due to a strong sorption affinity for PCP.

• The inhibition of biochar on PCP degradation was weaker in anaerobic than in aerobic condition.

• Biochar stimulated the growth of aerobic PCP-degrading bacteria Bacillus and Sphingomonas.

• Facultative organohalide-respiring bacteria were the PCP degraders under anaerobic conditions.

Abstract

Organochlorines are critical soil contaminants and the use of biochar has recently shown potential to improve soil remediation. However, little is known about biochar-microbe interactions nor the impact on environmental processes such as the immobilization and biodegradation of organochlorine compounds. In this study, we performed microcosm experiments to elucidate how biochar affected the biodegradation and sequestration of pentachlorophenol (PCP). Our results showed that the amendment of biochar markedly inhibited PCP biodegradation due to a strong sorption affinity for PCP under both aerobic and anaerobic conditions. Notably, the inhibitory effect was relatively weaker under anaerobic conditions than under aerobic conditions. The addition of biochar can dramatically shift the bacterial community diversity in the PCP-spiked soils. Under aerobic conditions, biochar significantly stimulated the growth of PCP-degrading bacteria Bacillus and Sphingomonas, but reduced the opportunities for microbes to contact with PCP directly. Under anaerobic conditions, the non-strict organohalide-respiring bacteria Desulfovibrio, Anaeromyxobacter, Geobacter and Desulfomonile were the main drivers of PCP transformation. Our results imply that the use of biochar as a soil remediation strategy for organochlorine compounds should be cautious.

Introduction

Organochlorine compounds (OCs) have played a key role in modern agriculture and industry, providing agronomic and economic products as herbicides, insecticides, fungicides and solvents (Cheng et al., 2018). However, OCs are critical soil contaminants due to its toxicity to plants, animals and humans, through environmental accumulation (Cai et al., 2013; Zhu et al., 2019a). Chemical, physical and biological methods have been applied to increase the removal of OCs in the environment (Czaplicka, 2004; Izanloo et al., 2019; Salimi et al., 2019). Usually, photodegradation that catalyzed by TiO₂ composites and stabilization that mediated by synthetic sorbents are main contaminant removal means in wastewater treatments (Piranshahi et al., 2017; Sedghi et al., 2016). While in soil environment, microbial degradation is often the most important process for the natural attenuation of OCs. The extent of biodegradation and the fate (e.g. transport and transformation) of OCs are largely controlled by their bioavailability and mobility in soils. For instance, due to a low availability and high toxicity to soil microorganisms, OCs such as polychlorinated biphenyls (PCBs) are highly recalcitrant to degrade and have half-life in soils measured in decades (Correa et al., 2010). In order to meet remediation needs in the most cost-effective manner, understanding the regulation of mobility and bioavailability among OCs, soil particles and the functional microbes has become an imperative for engineering natural processes.

Soil organic carbon is a critical factor controlling the fate of OCs (Yang et al., 2010). In particular, biochar, a special type of organic carbon, has received a considerable attention since it is widely distributed in agricultural lands and comprised of up to 80 % organic carbon in soils (Dai et al., 2016). Biochar is considered to be an effective amendment for the soil remediation (Kuppusamy et al., 2016). Recent studies demonstrated that biochar affects microbial activity, and alters soil microbial community structure and abundance (Awasthi et al., 2017; Lundberg and Sundqvist, 2011; Tong et al., 2014; Zhu et al., 2017). However, the available conclusive results from previous studies regarding biochar-microbe interactions on the mobility and bioavailability of OCs were inconsistent (Jones et al., 2011; Lou et al., 2011; Tong et al., 2014). Several studies revealed an inhibiting influence of biochar on pesticide degradation by reducing the availability of pesticide to soil microbes (Jones et al., 2011; Song et al., 2012); while Qin et al. (2013) showed an opposite result that the removal efficiency of contaminant was significantly enhanced in soils when amended with biochar.

Because of its large surface and high microporosity, biochar is considered to be a “supersorbent”, particularly effective in sorption and sequestration of organic and inorganic contaminants in soil environment (Cao et al., 2009). Sorption is an important pathway for removal of environmental pollutants, e.g. the adsorption of pesticides that mediated by synthetic sorbents in aquatic ecosystem (Bagheri et al., 2019; Behbahani et al., 2013). The great sorption/sequestration ability of organic contaminants onto the biochars greatly lowers the toxicity and mobility of pollutants in the soil, and also lead to a decrease in the bioavailability of OCs for bioremediation (Xu et al., 2012; Yu et al., 2009). Jones et al. (2011) showed that typical agronomic application rates of 10-100 t ha⁻¹ of hardwood-derived biochar significantly decreased the biodegradation and leaching of simazine in two agricultural soils. This is likely induced by a high sorption of simazine onto the biochar, which consequently limited its bioavailability to the indigenous microbial communities. While numerous studies in past decades have focused on the soil applications of biochar with its stabilization of OCs (Lou et al., 2011; Yang et al., 2010), the influence of biochar on the soil microbial community structure and function during biodegradation is still unclear.

Recent studies have demonstrated that biochars are able to act as electron shuttles to microorganisms and promote pollutant degradation (Klüpfel et al., 2014; Yu et al., 2015). For instance, Yu et al. (2015) exhibited the findings that the presence of biochar greatly enhanced the microbial transformation of pentachlorophenol (PCP), among which biochar could potentially act as an electron conduit for Geobacter sulfurreducens during biodegradation. Biochar can also enhance the transformation of OCs through reshaping the microbial community structures and promoting the growth and metabolism of functional microbes in the contaminated soils (Tong et al., 2014). It is interesting to note that biochars produce an opposite effect on microbial degradation of organic pollutants, that is, when acting as sorbents, the degradation of OCs would be limited due to its high sorption ability, while the microbial degradation of OCs would be enhanced when acting as conduits for electron transfer or growth stimulants. However, the available previous studies were mainly focus on only one aspect of the roles biochar played during degradation of OCs (Klüpfel et al., 2014; Xu et al., 2012; Yu et al., 2009), a systematic investigation is, hence, necessary to thoroughly evaluate which pathway is dominant, and if dominant, to what extent, during the total contribution of biochar in influencing OC degradation.

PCP, an ionizable chlorinated pollutant, is widely applied in agricultural and industrial applications such as insecticides and wood preservatives (Xu et al., 2015). Biodegradation is the most important process for the removal of PCP in the soil environment. Contrasting mechanisms are involved for microbial degradation of PCP under aerobic and anaerobic conditions (Bosso and Cristinzio, 2014). Bacteria can destruct the aromatic ring of PCP to CO₂ through the oxygenase process under aerobic condition. While under anaerobic condition, PCP can be transformed through reductive dechlorination process, where PCP acts as an electron acceptor. As a widely used remediation material, biochar would have an impact on PCP biodegradation due to its high sequestration and electron transfer ability. Hence, this study investigated what impacts of rice husk-derived biochar possess on the transformation of PCP in soils under both aerobic and anaerobic environments, through combination of both processes of dynamic analysis and molecular-based methods. Our study aimed to (i) illustrate the influence of biochar on abiotic and biotic PCP degradation, (ii) demonstrate the effect of biochar on the microbial community structure and function and (iii) understand the effects of biochar-microbe interactions on the environmental fate of PCP.