The anionic surfactant sodium lauryl ether sulfate (SLES) is the main component in most foaming agents (FAs) used in the excavation of highway and railway tunnels with Earth pressure balance-tunnel boring machines (EPB-TBMs) (Barra Caracciolo et al., 2017). FAs are used to change the mechanical properties and hydraulic behavior of soil, ensuring a malleable material that can be manageably excavated and transported to temporary areas (Peila, 2014; Peila et al., 2016). Due to the numerous tunneling projects currently in progress, several hundreds of millions of tons of soil debris (spoil material) are produced worldwide annually, raising the question of how to handle and dispose of them (Rahimzadeh et al., 2018; Rolando et al., 2020). Surfactants, including SLES, can be toxic for aquatic ecosystems if present at concentrations higher than the critical micellar one (Barra Caracciolo et al., 2017; Mariani et al., 2020; Rolando et al., 2020). The presence of SLES in spoil material can influence its recycling as a by-product; in fact, if the residual concentration of SLES is high, there can be toxic effects.

Previous experiments conducted on spoil material from tunnel excavation sites demonstrated that SLES was not toxic for terrestrial organisms (e.g., Lepidium sativum and Eisenia fetida) (Galli et al., 2019). However, in some cases, it showed detrimental effects on two aquatic species (Pseudokirchneriella subcapitata and Aliivibrio fischeri) (Grenni et al., 2018; Finizio et al., 2020; Patrolecco et al., 2020; Barra Caracciolo et al., 2021). Interestingly, the bacterium A. fischeri was shown to be very sensitive to SLES residues. In fact, a positive correlation between SLES concentrations and a toxic effect (inhibition of bioluminescence) on the bacterium was found in a 2-year monitoring of the spoil material from a highway construction site, making it possible to establish 2 mg/L as a “threshold value” of the toxic effect in the elutriates produced from spoil material (Mariani et al., 2020).

Reducing waste production and reusing by-products are the primary objectives of the “circular economy,” and in this context, the biodegradation of SLES becomes a key question in the safe reclaiming of excavated soils. Currently, tunnel debris can be used for refilling old quarries, road constructions, and green areas and as a raw material for industrial production (Bellopede and Marini, 2011).

Sodium lauryl ether sulfate has been shown to be a biodegradable compound in soils from tunnel excavation sites, but with highly variable degradation rates (Barra Caracciolo et al., 2019, 2021). In fact, concentrations of SLES in the range of 27–350 mg/kg showed variable half-lives (DT₅₀) from 8 to 46 days (Finizio et al., 2020). These results were ascribable not only to the initial SLES concentrations but also to site-specific characteristics such as soil texture, depth, structure, mineralogy, microbial abundance, water content, and temperature, which influenced its biodegradation differently.

Although a natural attenuation (with no human intervention) of SLES is expected due to the environmental microorganisms present in the excavated soil, degradation times cannot always meet construction site requirements. In some cases, the spoil material can be temporarily stored at the construction site for the time needed for SLES biodegradation (Barra Caracciolo et al., 2019). This practice was successfully used in a recent tunnel construction site in Italy (Mariani et al., 2020). Unfortunately, in other cases, such as tunneling for a metro inside a city, an area for spoil material temporary storage is not available. In this case, the excavated materials have to be considered waste, requiring transportation, treatment, and disposal, with a significant increase in project costs and unnecessary landfill use (Barra Caracciolo et al., 2017; Rahimzadeh et al., 2018; Patrolecco et al., 2020).

In Italy, spoil material can be classified as a by-product if the chemical thresholds for some organic and inorganic contaminants (e.g., heavy metals, hydrocarbons C > 12) are not exceeded (Italian Decree, 2017). However, there are no SLES soil concentration limits (Annex 4 of the Italian Decree 120/2017) in EU and national legislation (Italian Decree, 2017). Consequently, the possibility that soil debris can be really considered a safe by-product is strongly related to SLES persistence and their residual concentrations, which in turn depend on abiotic and biotic site-specific conditions.

Sodium lauryl ether sulfate degradation is common in environmental bacteria able to resist the toxic effects of SLES and to degrade it (Barra Caracciolo et al., 2019). Several Gamma-Proteobacteria possess esterase enzymes that are able to break the SLES ester bond (Bornscheuer, 2002; Panda and Gowrishankar, 2005). In a recent previous work, a bacterial consortium (BC) capable of degrading completely pure SLES within 24 h was selected using enrichment cultures. The BC consisted of Gamma-Proteobacteria (99%), and the predominant (ca. 90%) genus was Pseudomonas (Rolando et al., 2020).

The aim of the present work was to test if adding the SLES pre-grown microbial culture (BC) to spoil material from a tunnel construction site enhanced the removal of the anionic surfactant residues, with potentially significant economic and environmental benefits.

The aim of the present work was to test the capability of a previously isolated BC to enhance SLES degradation, in FA-conditioned soil collected from a tunnel construction site, in order to verify its possible use for routine bioaugmentation purposes. Bioaugmentation is a green technology used successfully for bioremediation of soil and water from several contaminants (e.g., petroleum hydrocarbons and pesticides) (Gentry et al., 2004; Abatenh et al., 2017; Arora, 2018). It consists in adding exogenous microbial populations or autochthonous ones (as in this work) with the catabolic potential to remove specific pollutants, such as pesticides (Plangklang and Reungsang, 2011; Sun et al., 2020). One advantage of bioaugmentation is that the degradation process starts as soon as specific microbial degraders are introduced (Wu et al., 2019). The success of bioaugmentation depends on the ability of the inoculated microorganisms to continue their activity in the environment as long as necessary for contaminant removal. However, if the degradation times are relatively long (such as in the case of pesticides), competitive interactions with non-degrading microbial populations can occur, and specific environmental conditions can limit bioaugmentation efficiency during in situ remediation (Hibbing et al., 2010; Asok and Jisha, 2012; Stelting et al., 2014; Cavinato et al., 2017).

The fact that in our work the bacterial populations were isolated from the same soil and that SLES removal times were very low made this bioremediation strategy an example of a real nature-based solution.

Although there are several works (Cycoń et al., 2017; Nur Zaida and Piakong, 2018; Tondera et al., 2021) dealing with contaminant removal by bioaugmentation, most of them have been performed using culture media and/or in liquid media and at concentrations which do not reflect those found in real contamination scenarios (Silva et al., 2004). There are few works in which adding microbial strains to soil improved degradation of organic contaminants in field studies or directly in environmental soil samples. Bioaugmentation can be applied using single microbial populations or a microbial consortium. For example, microbial consortia have been reported to degrade oils in polluted soil (Silva-Castro et al., 2012), in waste lubricating oil (Bhattacharya et al., 2015), in seawater (Dellagnezze et al., 2016), and in petroleum hydrocarbon in contaminated groundwater (Poi et al., 2018) and triazines in water and soil (Nasseri et al., 2014; Sagarkar et al., 2014). Triazine degradation has been performed in several bioaugmentation experiments with concentrations of these herbicides much higher than those commonly found in soil, such as in the study by Silva et al. (2004). However, in a recent work, Chen et al. (2021) showed the capability of a single bacterial population to degrade atrazine in a real contaminated soil (Chen et al., 2021).

Most works on anionic surfactants are aimed at evaluating biodegradation of sodium dodecyl sulfate, linear alkylbenzene sulfonate, and SLES in activated sludge (Hosseini et al., 2007), industrial wastewater (Karray et al., 2016; Fedeila et al., 2018), municipal wastewater (de Faria et al., 2019), and wastewater treatment plants (Paulo et al., 2017), because they are contaminants widely used in cosmetics, cleaning products, and personal care products (Barra Caracciolo et al., 2017; Hashim et al., 2018).

On the other hand, there have been no bioaugmentation experiments for remediating SLES, except for the work by Dhouib et al. (2003). These authors found a bacterial population of Gamma-Proteobacteria (Citrobacter braakii) that was able to degrade high concentrations of SLES in an enrichment culture using wastewater samples from a cosmetic plant as the inoculum. This work supports our results and the role of Gamma-Proteobacteria class in removing this anionic surfactant. Interestingly, in our study, where the soil came from a real construction site and the surfactant concentrations (130 mg/kg) were those used for the excavation, the bioaugmentation of the spoil material with the BC significantly (sixfold) improved the natural degradation time of SLES. Moreover, from an applied perspective, using a microbial consortium rather than a pure culture is more advantageous because it provides the metabolic diversity and robustness needed for field applications (Tyagi et al., 2011).

Finally, the ecotoxicological results confirmed the depollution of the soil (SLES in elutriates did not exert any toxicological effect) and the high sensitivity of A. fischeri to SLES residues higher than 2 mg/L (before SLES degradation), in line with the findings of previous works (Mariani et al., 2020; Patrolecco et al., 2020). The use of this ecotoxicological test in supporting chemical analysis is very powerful because it is an effective tool that can evaluate an overall matrix toxicity including chemicals (e.g., possible metabolites and/or unknown elements present in soil) non-directly analyzed. Other studies used A. fischeri as an effective screening test for soil samples (Parvez et al., 2006; Abbas et al., 2018).

Bioaugmentation with the BC identified at a construction site makes it possible to remove anionic surfactant residues and clean up spoil material in a few hours, ensuring a safe by-product and saving execution time and overall costs for the tunneling industry. To our knowledge, this study is the first using a SLES-degrading BC for bioaugmentation purposes in a contaminated soil from a real environmental scenario. This remediation strategy is a promising low-cost and nature-based solution, for a prompt and safe reuse of the spoil material, avoiding its temporary storage and unnecessary waste production and transfer to landfills. This technique could be used, e.g., in the case of metro tunneling inside a city or through mountains along a sea coast, where the lack of space prevents temporary storage of the spoil material for its natural attenuation. The overall results show how a diversified approach involving chemical, microbiological, and ecotoxicological assessments of polluted soil can improve our understanding of the biodegradability of pollutants in bioremediation strategies. Further studies are in progress for finding the best practice (e.g., alginate microspheres) for seeding the BC on a large scale in construction sites.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

LR, AB, PG, LM, JR, FS, GG, AV, and LP: methodology, formal analysis, and validation. LR and AB: writing, original draft preparation, and editing. AB, PG, and LP: supervision. AB: funding acquisition. All authors have read and agreed to the published version of the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.