Enhanced remediation of PAHs-contaminated site soil by bioaugmentation with graphene oxide immobilized bacterial pellets
Graphical Abstract
Introduction
Soil pollution caused by polycyclic aromatic hydrocarbons (PAHs) has become one of the main environmental problems faced currently by most countries in the world. Especially in China, the point exceeded rate of PAHs in soil has reach up to 1.4%. Therefore, it is quite urgent to develop high-efficiency and sustainable remediation strategies for cleanup of these pollutants in soil environment. Bioremediation has gradually attracted increasing attention because of many advantages, such as economic, green, environmentally friendly and so on, particularly microbial bioaugmentation technology (Liao et al., 2019, Sun et al., 2012). However, artificially added degrading bacteria are often difficult to resist high-concentration pollution stress, complex environmental conditions (e.g., extreme pH and high salt) and competition from indigenous microbial communities, resulting in a rapid decrease in abundance of added degrading bacteria and low degradation efficiency of PAHs (Stefaniuk et al., 2018, Suszek-Lopatka et al., 2019, Zeng et al., 2021).
Immobilization technology is one of important ways to solve this problem by providing more comfortable shelter for degrading bacteria. A large number of immobilized materials, including biochar (Bandara et al., 2019, Deng et al., 2021), polyvinyl alcohol (Chen et al., 2021), sodium alginate (Ravikumar et al., 2016), organoclay (Kim et al., 2012) and chitosan/alginate (Dou et al., 2021), etc., have been explored for the improvement in removal efficiency of organic pollutants in complex environment. Compared with other materials, sodium alginate, with many advantages including high biocompatibility and low toxicity, has been considered as an excellent microbial immobilization carrier for growth and proliferation of degrading bacteria in water treatment or wastewater field (Dai et al., 2020, Nie et al., 2015; Park et al., 2021). However, sodium alginate is still comparatively vulnerable to ruptures and maintain limited protective effect in more complex soil environment. In addition, relatively small adsorption ability of sodium alginate for pollutants is one of crucial factors influencing removal efficiency of pollutants by embedded degrading bacteria (Dai et al., 2020, Ouyang et al., 2021). Although some high hardness materials (e.g., Fe and polyvinyl alcohol) have been investigated to enhance mechanical strength of sodium alginate (Chen et al., 2021, Funada et al., 2018, Shanker et al., 2017), effective materials for promoting removal of PAHs in soil environment remain still relatively limited. Therefore, developing novel immobilized bacterial agents with higher mechanical strength and stronger adsorption performance are urgently needed in bioremediation of contaminated soil, especially highly-contaminated site soil.
In recent years, nanomaterials have displayed great potential to remove or transform recalcitrant pollutants in complex environmental media due to their unique features of large specific surface area, high reactivity, selectivity and versatility, which is attracting an increasing research and industrial attentions (Fernando et al., 2020, Ge et al., 2018, Queiroz et al., 2021). Graphene oxide (GO), as a typical carbon nanomaterial, harbors an excellent adsorption ability for PAHs, especially high-molecular-weight PAHs, due to the strong interaction with the carboxyl groups attaching to the edges of GO (Wang et al., 2014, Zhang et al., 2013). Besides, the addition of GO has been observed to augment the mechanical strength and chemical stability of alginate hydrogels (Choe et al., 2019, Valentin et al., 2019). Alginate-GO composite-based thin films and hydrogel beads have been explored in many fields (Zhu et al., 2017), such as water purification (Yang et al., 2018). Moreover, our previous study demonstrated that GO was highly biocompatible for resistant bacteria and able to promote the growth and biofilm formation of Paracoccus aminovorans HPD-2, a high-efficiency PAH-degrading bacterium (Mao et al., 2020). Therefore, we hypothesized that GO-immobilized bacterial agents, prepared by embedding PAH-degrading bacteria in alginate-GO nanocomposites, could better protect degrading bacteria from stress of complex soil environment and enhance the degradation of high-concentration PAHs in site soil.
The objectives of this study were to (1) develop novel high-efficiency nano-immobilized bacterial pellets for bioaugmentation in PAH-contaminated site soil; (2) decipher the underlying mechanisms driving the promotion effect of the nano-immobilized bacterial pellets. To address these objectives, nano-immobilized bacterial pellets were constructed by embedding a high-efficiency PAH-degrading bacterium in alginate-GO nanocomposites. A series of physical, microscopic and spectroscopic technologies were applied to characterize the bacterial pellets. Microcosm culture experiments were performed with a high-concentration-PAH- contaminated site soil spiked with different types of bacterial pellets. High-throughput sequencing and real-time PCR were used to investigate the changes in bacterial community structure and abundance of functional genes.
Section snippets
Materials
Single-layered GO nanosheets were purchased from Nanjing XF Nano Material Technology Co., Ltd., China. The characteristics of GO have been demonstrated in our previous study (Mao et al., 2020, Ren et al., 2019). In brief, GO has a flat surface with multiple oxygen containing functional groups, mainly including OH, CH3 and CC groups. The carbon and oxygen content are 65.93% and 32.00%, respectively. The BET specific surface area, average pore size and average thickness are 237.7 m2/g, 17.92 nm
Characterization of GO-immobilized bacterial pellets
GO immobilization had no influence on the diameter and density of bacterial pellets. All the bacterial pellets of four treatments are about 3.0 mm in diameter and have a density of 1.00 g cm-3 (Fig. 1a-b). Compared with the traditional bacterial pellets (J), JGO and JGOLB could promote the tolerable pressure of bacterial pellets by 3 and 2-fold, respectively (Fig. 1c). Elastic modulus was also characterized for the three bacterial pellets using AFM. The elastic modulus of traditional bacterial
Discussion
In this study, a novel type of nano-immobilized PAHs-degrading bacterial pellets was constructed by embedding high-efficiency degrading bacteria Paracoccus aminovorans HPD-2 in nanocomposite of GO, alginate and LB medium. Compared with traditional bacterial pellets, GO-immobilized bacterial pellets displayed superior mechanical performance, surface properties and mass transfer ability. Furthermore, results from microcosm culture experiment revealed JGOLB treatment significantly increased the
Conclusion
A novel type of GO-immobilized bacterial pellets (JGOLB) was successfully prepared by encapsulation of degrading bacteria in alginate-GO-LB nanocomposites. The GO-immobilized bacterial pellets displayed superior properties compared with traditional alginate-based bacterial pellets, such as higher mechanical strength, larger surface area and increased mesopore volume. Compared to traditional bacterial pellets, JGOLB caused a significant increase in the abundance of embedded degrading bacteria in
CRediT authorship contribution statement
Wenjie Ren, Ying Teng and Yongming Luo conceived and supervised the projects. Wenjie Ren designed the experiments. Haoran Liu and Tingyu Mao performed the experiments. Wenjie Ren, Haoran Liu and Rui Zhao analyzed data. Wenjie Ren and Haoran Liu wrote the manuscript. Ying Teng and Yongming Luo revised the manuscript.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was jointly supported by the National Key Research and Development Program of China (2017YFA0207001), the National Natural Science Foundation of China (41877139), the Major Projects of the National Natural Science Foundation of China (41991335), the Ecological and Environmental Research Program of Jiangsu Province, China (2020001), and the Open Project of the Technology Innovation Center for Ecological Monitoring & Restoration Project on Land (Arable), Ministry of Natural Resources (
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