Responsiveness change of biochemistry and micro-ecology in alkaline soil under PAHs contamination with or without heavy metal interaction

Highlights

• Cd existence contributed to the dissipation of pyrene in soil.

• Cd presence helped microorganisms adaption under high level pyrene stress.

• Resistance microbe enrichment contributed to nature attenuation of pyrene pollution.

• Cd contributed to soil microbial diversity maintenance under high pyrene stress.

Abstract

Co-presence of organic pollutants and heavy metals in soil is causing increasing concerns, but the lack of knowledge of relation between soil ecology and pollutant fate is limiting the developing of specific control strategy. This study investigated soil change under pyrene stress and its interaction with cadmium (Cd). Soil physicochemical properties were not seriously influenced. However, pollutants’ presence easily varied soil microbial activity, quantity, and diversity. Under high-level pyrene, Cd presence contributed to soil indigenous microorganisms’ adaption and soil microbial community structure stability. Soils with both pyrene and Cd presented 7.11–12.0% higher pyrene degradation compared with single pyrene treatment. High-throughput sequencing analysis indicated the proportion of Mycobacterium sp., a commonly known PAHs degrader, increased to 25.2–48.5% in treatments from 0.52% in control. This phenomenon was consistent with the increase of PAHs probable degraders (the ratio increased to 2.86–6.57% from 0.24% in control). Higher Cd bioavailability was also observed in soils with both pollutants than that with Cd alone. And Cd existence caused the elevation of Cd resistant bacterium Limnobacter sp. (increased to 12.2% in CdCK from 2.06% in control). Functional gene prediction also indicated that abundance of genes related to nutrient metabolism decreased dramatically with pollutants, while the abundances of energy metabolism, lipid metabolism, secondary metabolites biosynthesis-related genes increased (especially for aromatic compound degradation related genes). These results indicated the mutual effect and internal-interaction existed between pollutants and soils resulted in pollutants’ fate and soil microbial changes, providing further information regarding pollutants dissipation and transformation under soil microbial response.

Introduction

Soil is a vital resource for the human race, whose conditions influence not only food production, but also environmental processes (Trasar-Cepeda C, 2000). Nowadays, large numbers of contaminants are entering soil and threatening the ecosystem (Chen et al., 2015a).

Soil microorganism is crucial for the ecological functions of soil, which influences nutrient cycles and transformation in soil. The metabolism of soil microorganisms is vital for organics degradation and could also mediate element transformation. When the external environment changes under fertilization, mining, or contamination, the soil microbial organisms would respond accordingly, which makes them suitable to evaluate soil quality (Wang et al., 2018). Contamination could seriously affect soil microbial structure and activities (dos Santos et al., 2012). The variation of soil microbial structure and activity will in return impact the passivation and transformation of pollutants (Gianfreda and Rao, 2008). Understanding their relationship would benefit the investigation of soil ecological response and the fates of pollutants.

Polycyclic aromatic hydrocarbons (PAHs) are toxic, mutagenic, and carcinogenic compounds widely distributed in the environment, which can resist nucleophilic attacks and persist in soil (Bharatkumar Patel et al., 2018). Under PAHs pollution, the soil microbial composition and activity could be altered, soil biochemical property could be changed, which will in return influence the fates of PAHs. In many mining and metallurgy industries sites, PAHs commonly co-present with heavy metals like Cadmium (Cd) (Khan et al., 2017; Lu et al., 2014). Their combined presence would influence the soil property differently, which would affect their fates due to the interaction among different compounds and soil biota (Wu et al., 2019). Therefore, it is necessary to consider heavy metal co-existence when investigating PAHs influence on the soil ecosystem. Pyrene is one representative high molecular weight (HMW) PAHs which has been frequently investigated as a model pollutant (Sivaram et al., 2018; Wu et al., 2019). In this study, when investigating pyrene’s influence on soil, the toxic nonessential heavy metal Cd was chosen to understand its impaction on pyrene fate and their synthetical influence on soil micro-ecosystem.

Previous studies have focused on pollutants’ influence on soil microorganisms during various remediation processes (Kaczynski et al., 2020; Lin et al., 2019), which could not give a clear view of microbial response and pollutant fate during natural attenuation. The study of soil microbial community variation under co-contamination was rare, let alone the fates of pollutants under these multiple interactions. This study aims to investigate soil microbial response under pyrene stress and pyrene dissipation with or without Cd. Soil physicochemical and biochemical property changes were explored. Pollutant formation variation was also evaluated using various extraction measures. High-throughput sequencing and microbial functional genes prediction techniques were applied to further understand the soil microbial variation under pollutant stress. This study will expand the current knowledge about the ecological effect of PAHs and the fate of the pollutants under this interaction, which will provide an insight into the better soil contamination control strategy.