Original Research
Bioremediation perspective of historically contaminated sediment with polycyclic aromatic hydrocarbons

https://doi.org/10.1016/j.ijsrc.2020.11.004Get rights and content

Abstract

The purpose of the current study is to compare the influence of different aerobic conditions (biostimulation (BS), bioaugmentation (BA), and a combination of biostimulation and bioaugmentation (BB)) on polycyclic aromatic hydrocarbons (PAH) degradation and compare the degraded amount with single step XAD-4 extraction as a new tool for bioavailability assessment for chronically contaminated sediment samples obtained from territory of Autonomous Province Vojvodina of Serbia (S1, S2, and S3). A great number of papers dealing with biodegradation of PAHs in spiked sediment or soil have been published, but to the authors’ knowledge, a limited number of papers studied aged, historically polluted sediment and a sum of chosen U.S. Environmental Protection Agency (USEPA) PAHs. A significant reduction (up to 67%) in PAH concentration was observed, while the percentage of reduction varied depending on the sediment sample and treatment used. BS treatment successfully stimulated growth of indigenous bacteria. Further, PAH-degrading strain Sphingomonas paucimobilis F8 inoculated in BA and BB treatment survived for up to 7 weeks after it was suppressed by unfavorable conditions or native microbes. Degraded amounts generally showed good correlation with results obtained from XAD-4 extraction. Results obtained in the current study represent a good start for standardizing a XAD-4 extraction technique as a simplified, easier, and lower cost method for bioavailability assessment.

Introduction

Polycyclic Aromatic Hydrocarbons (PAHs) are a class of serious environmental pollutants with high mutagenic and carcinogenic potential, and belong to a ubiquitous group of several hundred chemicals with various structures and varied toxicity (Maletić et al., 2019; Wu et al., 2020). PAHs belong among hydrophobic organic contaminants that tend to adsorb onto soil and sediment matrices and have poor bioavailability after their arrival in the soil and sediment (Kuppusamy et al., 2017; Maletić et al., 2019; Zhao et al., 2016). Their physical and chemical properties determine and have influence on their fate in the environment, including their mobility by means of reverse desorption into aquatic systems or their microbial biodegradability (Kuppusamy et al., 2017; Maletić et al., 2019). A large number of studies have used freshly spiked sediment (Gomez-Eyles et al., 2010; Wang et al., 2017), thus, neglecting the effect of aging and interaction with the organic matter and clay present. As organic compounds age in soil or sediment they become less available for uptake by organisms, and are, thus, less likely to have toxic effects or be degraded by soil microorganisms (Alexander, 2000; Grgić et al., 2019). The biological effects of a contaminant are, therefore, not related to its total concentration, but to the bioavailable fraction. This is the fraction of the contaminant that is biologically available for uptake (Alexander, 2000; Duan et al., 2016; Gomez-Eyles et al., 2010; Posada-Baquero et al., 2019), so researchers have used contaminant bioavailability in sediment as the foundation to assess environmental risk and to predict bioremediation efficiency (Duan et al., 2016; Li et al., 2016; Rončević et al., 2016; Spasojević et al., 2018).

Strategies and approaches including chemical, physical, and biological strategies have been optimized and utilized to improve PAH degradation and bioavailability in polluted sediment (Kuppusamy et al., 2017; Soleimani, 2012). Based on the possibility of accessibility and biodegradation assessment of organic contaminants in the environment a numerous biological methods which use microorganisms are developed for characterization of organic contaminant bioavailability (Martín-Díaz et al., 2009; Zhao et al., 2014). Bioremediation has been shown to be a cost effective and environmentally friendly approach to remediate contaminated sites (Alegbeleye et al., 2017; Soleimani, 2012). Several bacterial genera Pseudomonas, Sphingomonas, Mycobacterium, Ralstonia, and others (Haleyur et al., 2019; Juárez Tomás et al., 2019; Juhasz & Naidu, 2000; Kaczorek et al., 2013; Ramadass et al., 2018; Redfern et al., 2019; Song et al., 2011; Tøndervik et al., 2012; Wu et al., 2020; Zhang et al., 2011; Zhong et al., 2011) and fungal species such as Aspergillu ssp., Trichocladium canadense, and Fusarium oxysporum (Kadri et al., 2017; Silva et al., 2009) capable of degrading PAH compounds have been isolated and characterized.

To date, the regulation framework uses only the total-extractable concentrations of organic compounds in an environmental medium to assess their toxicity. However, researchers have proposed a new, simplified approach for toxicity and bioavailability assessment (Ortega-Calvo et al., 2015). In this context, there are some important questions to be answered on how to measure the bioavailable fraction. Physico-chemical extraction techniques predict the biodegradable fraction of contaminants using the process of rapid desorption of pollutants from solid media (Cachada et al., 2014; Gomez-Eyles et al., 2010; Riding et al., 2013; Spasojević et al., 2015). These techniques can be correlated with bioavailability to microorganisms capable of degrading the contaminants (Bernhardt et al., 2013; Haleyur et al., 2019; Posada-Baquero et al., 2019; Rončević et al., 2016; Spasojević et al., 2015). Many different physico-chemical techniques using Tenax, hydroxypropyl-β-cyclodextrin (HPCD), methyl-β-cyclodextrin (MCD), XAD-4, a commercially available polymeric adsorbent, or Triton X-100 to predict PAH bioavailability (Bernhardt et al., 2013; Burkhardt et al., 2005; Cuypers et al., 2002; Guo et al., 2016; Leech et al., 2020; Posada-Baquero et al., 2019; Spasojević et al., 2015; Sun et al., 2014) have been proposed to predict bioavailability in recent studies due to lower costs and improved timeliness.

Although there are numerous advantages in using these extraction methods there is a long way to go for these approaches to be established in environmental regulations. When correlating chemical predictors of bioavailability for bioassays it is important to consider that the bioavailability being measured is specific to the organism used in that particular bioassay, and also to be aware that the determination of earthworm or plant accumulation does not necessarily measure contaminant bioavailability, but rather measures an interaction end-point between the organism and the compound (Gomez-Eyles et al., 2010; Hickman & Reid, 2005; Leech et al., 2020; Posada-Baquero et al., 2019). The bioaccessibility of PAHs in historically polluted sediment may differ significantly from that in the individual PAH-spiked sediments (Čvančarová et al., 2013; Spasojević et al., 2015). A great number of papers have studied biodegradation of PAHs in historically polluted soil and spiked sediment/soil (Čvančarová et al., 2013; Gou et al., 2019; Harmsen & Rietra, 2018; Leonardi et al., 2007; Smułek et al., 2020; Spasojević et al., 2015), but, to the authors' knowledge, a limited number of papers studied aged, historically polluted sediment and the biodegradation of the sum of chosen U.S. Environmental Protection Agency (USEPA) PAHs. Thus, the current study aims to compare how a range of different aerobic conditions (biostimulation, bioaugmentation and combined biostimulation and bioaugmentation), frequently tested as bioremediation techniques, predict PAH bioavailability in historically polluted sediment and compare them with chemical techniques using a single step XAD-4 extraction, as an easier and lower cost method for bioavailability assessment.

Section snippets

Sediments

Historically PAH contaminated sediment was obtained from three different locations, two sediment samples were taken from two locations at canal Begej-Klek-Itebej (S1 and S2) and one sample from canal Danube–Tisa–Danube Canal (DTD)-Bački Petrovac-Karavukovo (S3) (Republic of Serbia). All three locations are under direct anthropogenic influence and represent recipients of wastewater, sludge, and runoff from agricultural land. Dubovina et al. (2018) measured heavy metals and PAHs in the sediment

PAH source in aged contaminated sediment

The initial sediment samples were highly contaminated with PAHs (Table 3) with its total amount in the range of 4.77–10.0 mg/kg. For identification of sediment pollution source the Low Molecular Weight/High Molecular Weight (LMWPAH (2–3 rings)/HMWPAH (4–6 rings)) ratio was used. Kuppusamy et al. (2017) pointed out that if this ratio is <1, the PAH source is considered as pyrogenic, and if this ratio is >1, the PAH source is considered as petrogenic. LMWPAH/HMWPAH in the investigated sediment

Conclusion

Bioavailability assessment of historically polluted sediment is highly important, as this kind of pollution is a global problem considering the amount of sediment that needs to be remediated. During the bioremediation process, the bioavailable concentration provides more risk-based information than the total PAH concentrations only. The current study investigated a series of different bioremediation conditions for estimation of potentially bioaccessible fractions of PAHs, including

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

The authors gratefully acknowledge the support of the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. x451-03-68/2020-14/200125).

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