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Article

Investigating the Potential of River Sediment Bacteria for Trichloroethylene Bioremediation

1
Sustainability Cluster, School of Advanced Engineering, University of Petroleum and Energy Studies, Dehradun 248007, Uttarakhand, India
2
Department of Chemistry and Biochemistry, Texas State University, San Marcos, TX 78666, USA
3
Ingram School of Engineering, Texas State University, San Marcos, TX 78666, USA
*
Author to whom correspondence should be addressed.
Water 2024, 16(20), 2941; https://doi.org/10.3390/w16202941
Submission received: 21 August 2024 / Revised: 5 October 2024 / Accepted: 14 October 2024 / Published: 16 October 2024
(This article belongs to the Special Issue Biological Treatment of Water Contaminants: A New Insight)

Abstract

:
Trichloroethylene (TCE) is a prevalent groundwater contaminant detected worldwide, and microbes are sensitive indicators and initial responders to these chemical contaminants causing disturbances to their ecosystem. In this study, microbes isolated from San Marcos River sediment were screened for their TCE degradation potential. Among the twelve isolates (SAN1-12), five isolates demonstrated TCE degradation within 5 days at 25 °C and 40 mg/L of TCE concentration in the following order: SAN8 (87.56%), SAN1 (77.31%), SAN2 (76.58%), SAN3 (49.20%), and SAN7 (3.36%). On increasing the TCE concentration to 80 mg/L, the degradation efficiency of these isolates declined, although SAN8 remained the prominent TCE degrader with 75.67% degradation. The prominent TCE-degrading isolates were identified as Aeromonas sp. SAN1, Bacillus sp. SAN2, Gordonia sp. SAN3, and Bacillus proteolyticus SAN8 using 16S rRNA sequencing. The TCE degradation and cell biomass of Bacillus proteolyticus SAN8 were significantly improved when the incubation temperature was increased from 25 °C to 30 °C. However, both slightly acidic and alkaline pH levels, as well as higher TCE concentrations, lowered the efficacy of TCE degradation. Nevertheless, these conditions led to an increase in bacterial cell biomass.

1. Introduction

TCE is the chlorinated aliphatic hydrocarbon ubiquitously detected in soil and groundwater owing to inappropriate solvent handling, illegal disposal practices, and accidental spills [1,2]. TCE has been extensively used as a cleanser and degreaser agent in the industrial sector [3,4,5]. Due to the high molecular weight and low water solubility, TCE accumulates as dense non-aqueous phase liquids (DNAPLs), acting as a long-term secondary pollutant in groundwater pollution [3,6]. Chloroethene concentrations in groundwater near a source zone can range from solvent water solubility levels up to 1280 mg/L (~8.7 mM) for TCE, significantly exceeding risk-based maximum exposure limits for health [6]. Likewise, TCE adsorbed on mineral and organic constituents in sediments is slowly released back into the water, thus acting as a long-term pollutant in groundwater [2]. The European Commission, the United States Environmental Protection Agency, and the Ministry of Ecology and Environment of China have recorded TCE as a priority pollutant [7,8]. Being a Group 1 carcinogen, exposure to TCE increases the risk of cancer to the cervix, liver, kidney, and biliary passages, as well as non-Hodgkin lymphoma and esophageal adenocarcinoma [2,4,9]. In addition, TCE has been observed to have endocrine-disrupting effects, altering the reproductive system [10].
Several strategies, including adsorption, electrochemistry, and advanced oxidation, were studied and implemented for TCE remediation in water [8]. However, high operational costs and complicated installation processes hinder the wide applications of these technologies. However, microbial biodegradation has achieved widespread consideration from researchers owing to cost-efficiency, easy application, environmental friendliness, and sustainable perspective [11,12]. The TCE biodegradation processes can be broadly categorized into four main types for isolated bacteria and mixed microbial cultures: anaerobic reductive dechlorination, anaerobic co-metabolic reductive dechlorination, aerobic co-metabolism, and aerobic direct oxidation [2]. As the soil and water microbes are the sensitive indicators for chemical contaminants, they are the initial responders to chemicals entering their ecosystem [2]. To date, various researchers have indicated that TCE can be reduced biologically by indigenous microbial communities under anaerobic conditions to short-chlorinated byproducts, dichloroethylene isomers, vinyl chloride, and less-toxic ethene [13]. Therefore, exploring new indigenous microbial communities from the contaminated site is an effective way to reveal an approach for TCE remediation under anaerobic, aerobic, and other environmental conditions [14].
The current study was centered on isolating microbes from the sediment of San Marcos River, TX, USA, an area surrounded by active crude oil drilling activities. The isolated microbes were further investigated for their TCE-degrading potential in batch culture techniques, and the residual TCE concentration was analyzed using GC-MS. The prominent TCE degraders were identified and tested at varying temperatures, pH levels, and TCE concentrations to assess TCE degradation potential along with bacterial cell biomass.

2. Materials and Methods

2.1. River Sediment Sampling and Isolation of TCE-Degrading Microorganisms

River sediment samples were collected from the San Marcos River in Luling, Texas (29.66642° N, 97.65179° W), an area with enduring crude oil drilling events. Sediment sampling was performed using a hole digger screw soil sampler at a depth of nearly three feet below the water surfaces and placed into sterile plastic bottles. The samples were transported to the laboratory in a cooling box. For isolation of TCE degraders, a one-gram sediment sample was introduced into 100 mL 1X M9 media, spiked with 100 mg/L TCE (ACS reagent, ≥99.5% purity), and incubated at 25 °C for 48 h. Bacterial isolation was conducted by plating 100 µL of enriched culture on TCE–nutrient agar plates containing 100 mg/L TCE. These plates were sealed with parafilm stripes and incubated at 25 °C for 24 h. Twelve morphologically distinct colonies denoted as SAN1 to SAN12 were isolated, subsequently purified, and tested for their TCE degradation competence in liquid M9 media.

2.2. Screening of Sediment Bacteria for TCE Degradation under Batch Culture

The TCE degradation was performed in a 40 mL glass bottle consisting of 25 mL 1X M9 media, 0.05% glucose, and 0.01% yeast extract. This medium was spiked with 40 and 80 mg/L of TCE and inoculated with 1% v/v 12 h old bacterial cultures of SAN1 to 12, individually. Bottles were tightly sealed and incubated at 25 °C for 5 days on a rotor mixture rotating 360° at 30 rpm. The residual TCE concentration in the degradation medium was investigated using GC-MS. Furthermore, identification of the prominent TCE degraders was performed by amplifying the 16S gene using 27F (5′-AGAGTTTGATCMTGGCTCAG-3′) and 1492R (5′-TACGGYTACCTTGTTACGACTT-3′) primers, and PCR products were sequenced at Epoch Life Science, Inc., Missouri City, TX, USA, using the ABI platform (version 5.2).

2.3. Optimization of TCE Degradation Condition for Bacillus proteolyticus SAN8

The bacterial growth, metabolism, enzyme activities, and bioavailability of the contaminants could be significantly affected at different pH, temperature, and TCE concentrations [2]. Therefore, optimization of these factors was crucial for determining the growth condition requirements of the isolated bacteria to achieve maximum TCE degradation. The pH optimization was conducted within the range of 6 to 8 while holding a constant temperature of 25 °C. Conversely, the temperature was optimized at 25 °C and 30 °C, with the TCE concentrations varying between 40 and 120 mg/L while maintaining a constant pH of 7. All the experiments were performed in 40 mL glass sample bottles containing 25 mL of M9 medium (details in Section 2.2) to maintain a relatively small headspace volume, presumably to make cultures initially aerobic and oxygen-limited at some point during the incubation. The M9-TCE-medium was inoculated with 1% v/v 12 h old bacterial culture and the bottles were tightly fastened to maintain oxygen-limiting conditions and incubated at 25 °C for 5 days on a rotor mixture spinning 360° at 30 rpm. To analyze bacterial dry cell weight (DCW) and residual TCE concentration, samples were collected by sacrificing one set from the degradation media.

2.4. GCMS Analysis of TCE

The residual TCE concentration in the degradation medium was analyzed using GCMS (Agilent Technologies model 7890B, Santa Clara, CA, USA). Before analysis, the TCE solution was diluted to 25 ppm; considering the initial TCE concentration, this diluted solution was spiked with 2 ppb of 1-chlorobutane as a surrogate. A solid-phase microextractor (SPME) fiber covered with Carboxen/Polydimethylsiloxane (CAR/PDMS) was employed to extract analytes from the solution and separation was executed on Agilent Technologies 30 m × 0.25 mm capillary columns (HP-5MS). The initial oven temperature was held at 45 °C for 5 min, ramped to 100 °C at the heating rate of 10 °C/min, and held for 5 min at this temperature. The injector temperature was set to 270 °C, and splitless mode was used for injection. The TCE was monitored at m/z = 130, and residual concentration was calculated based on the calibration curve.

3. Results and Discussion

3.1. Screening and Identification of TCE-Degrading Bacteria Isolated from River Sediment

Using the TCE–nutrient agar plating approach, twelve bacterial isolates were obtained from the sediment sample of the San Marcos River (Luling, TX, USA). These isolates were consequently investigated for their growth and TCE degradation (40 and 80 mg/L) ability in batch culture experiments in liquid M9-medium under oxygen-limited environments. Among the twelve bacterial isolates tested for the growth and TCE degradation at the concentration of 40 mg/L, only five isolates, SAN1, SAN2, SAN3, SAN7, and SAN8, were able to grow in liquid M9-TCE-media. These five isolates, SAN8 (87.56%), SAN1 (77.31%), SAN2 (76.58%), SAN3 (49.20%), and SAN7 (3.36%), demonstrated significant TCE degradation within 5 days at 25 °C (Supplementary Figure S1), whereas the other seven isolates failed to grow in liquid M9-TCE-media. These five isolates were investigated for TCE degradation at a concentration of 80 mg/L. However, the TCE degradation efficiency of these isolates had slightly declined in SAN8 (75.67%), SAN1 (51.63%), SAN2 (44.38%), SAN3 (27.45%), and SAN7 (3.20%) (Figure 1a). Four prominent TCE-degrading isolates were identified as Aeromonas sp. SAN1, Bacillus sp. SAN2, Gordonia sp. SAN3, and Bacillus proteolyticus SAN8 through 16S rRNA sequencing. The gene sequences of these isolates have been deposited in GenBank under accession numbers OR480982 (SAN1), OR480983 (SAN2), OR480984 (SAN3), and PP405078 (SAN8). The phylogenetic tree of SAN1, SAN2, and SAN3 was constructed (Supplementary Figure S2a–c), and the phylogenetic tree of the most prominent TCE degrader Bacillus proteolyticus SAN8 is depicted in Figure 1b. The G-C content of the 16S rRNA gene sequence of isolate SAN8 was 54.3%.
Previous researchers have reported several TCE-degrading microorganisms, including Desulfotomaculum, Sphingomonas, Desulfuromonas, Clostridium, Flavobacterium, Nitrospira, Bacillus, Pseudomonas, and Acidovorax that were found in areas contaminated with TCE [15,16]. These microorganisms demonstrate the potential to degrade TCE, revealing the adaptability of native microorganisms to TCE contamination via the development of tolerance mechanisms and metabolic strategies for TCE degradation [2,17]. Furthermore, reductive dechlorination bacteria are key agents in the TCE-dechlorinating processes within TCE-contaminated sites [2,16]. In the present study, the prominent TCE degraders isolated from river sediment were Aeromonas, a facultative anaerobe [18], and Bacillus, which can be either aerobic or facultatively anaerobic [19]. These microbes were able to switch between aerobic and anaerobic metabolism, in contrast to Gordonia, which was strictly aerobic [20]. Therefore, under oxygen-limited conditions, the facultatively anaerobic isolates Aeromonas sp. SAN1, Bacillus sp. SAN2, and Bacillus proteolyticus SAN8 have proven higher TCE degradation. The Bacillus proteolyticus SAN8 showed a closely correlating growth pattern with Bacillus proteolyticus strain TD42, a facultative anaerobe capable of growing in both oxygen-rich and oxygen-deprived conditions [21]. In comparison, the aerobic Gordonia sp. SAN3 primarily utilized the available oxygen for initial growth and subsequent TCE degradation, and the TCE degradation decreased with time.

3.2. Time-Dependent Degradation of TCE by Bacillus proteolyticus SAN8

A time-dependent study for TCE degradation by Bacillus proteolyticus SAN8 revealed 5.36% TCE degradation on day 1; the degradation then further improved with time, reaching 74.80% degradation on day 5 at 25 °C at the TCE concentration of 80 mg/L (Figure 2). The gradual increase in microbial TCE degradation over time could be attributed to various factors, including adaptation time, enzyme induction, biofilm formation, population growth, TCE concentration, and environmental factors. In the existing study, the TCE-degrading medium was added with a small amount of glucose as an easily available carbon source for initial fast growth and cell biomass production. The addition of glucose potentially boosted the microbial biomass and activity, thus accelerating the TCE dechlorination. In the reductive dechlorination, glucose could serve as an electron donor to TCE, resulting in the sequential replacement of chlorine atoms and formation of less chlorinated compounds such as cis-DCE, trans-DCE, and VC, which are eventually converted to ethene [22].
Methanotrophs are well known for their ability to co-oxidize TCE via methane monooxygenase, which leads to the transformation of TCE into less harmful or more easily degradable intermediates [23,24]. If Bacillus proteolyticus SAN8 harbors enzymes analogous to monooxygenases, a similar co-oxidation mechanism could be potentially responsible for TCE transformation. Therefore, the co-oxidation of TCE in Bacillus proteolyticus SAN8 could be comparable to the process observed in methanotrophs that express various forms of methane monooxygenase. Oxygen-induced co-oxidation would explain the ability of SAN8 to reduce TCE, as these bacteria may not directly metabolize TCE but co-oxidize during the metabolism of other substrates, such as glucose [23,24]. However, further research into the enzymatic pathway of Bacillus proteolyticus SAN8 could confirm the existence of a monooxygenase enzyme that could co-oxidize TCE. Hence, studies using oxygenase-specific inhibitors and genomic or proteomic analysis could provide further evidence for this degradation mechanism.

3.3. Investigating the Influence of Different Factors on TCE Biodegradation

3.3.1. Effect of pH on TCE Degradation

The bacterial growth, enzyme activity, and metabolism could be greatly influenced by the pH of the degradation media. As depicted in Figure 3, the effect of degradation medium pH on Bacillus proteolyticus SAN8 was studied at pH 6, 7, and 8. At pH 6, the TCE degradation was recorded as 67.21% with a dry cell biomass (DCW) of 378 mg/L. The maximum TCE degradation of 78.76% was observed at pH 7 with a DCW of 430 mg/L. However, the TCE degradation performance decreased to 71.60% on raising the pH to 8, although the DCW further increased to 445 mg/L. Earlier studies have proven that TCE dichlorination rarely occurs when the degradation medium pH is below 6, while the optimum range was between pH 6.8 and 7.8 [3].

3.3.2. Impact of Temperature and TCE Concentration on Bioremediation

The bioavailability of hydrophobic and volatile contaminants is substantially affected by temperature, which ultimately affects bacterial bioremediation performance. The optimal TCE concentration is crucial for efficient bioremediation since high concentrations could be toxic, leading to suppression of bacterial growth and activities, while low concentrations may result in inefficient bioremediation. Therefore, the incubation temperature for Bacillus proteolyticus SAN8 was optimized at temperatures of 25 °C and 30 °C, with TCE concentration adjusted from 40 to 120 mg/L.
At 25 °C and a TCE concentration of 40 mg/L, the maximum degradation of 88.71% was achieved. However, increasing the TCE concentrations to 80 mg/L and 120 mg/L resulted in a decrease in the TCE degradation to 80.09% and 67.87%, respectively. The DCW gradually increased to 304 mg/L, 418 mg/L, and 461 mg/L, with TCE concentrations of 40, 80, and 120 mg/L, correspondingly (Figure 4a). Interestingly, on raising the temperature to 30 °C, the TCE degradation was enhanced to 91.20% at 40 mg/L TCE, 82.33% at 80 mg/L, and 69.12% at 120 mg/L TCE (Figure 4b). Similarly, the DCW increased from 351 mg/L to 502 mg/L with rising TCE concentration from 40 mg/L to 120 mg/L (Figure 4b). The increase in TCE degradation could correlate with the increased DCW detected with rising TCE concentrations and temperature. This phenomenon of improved DCW with temperature and TCE concentration might be related to exopolysaccharide (EPS) production, which shields bacterial cells from direct TCE toxicity.
In previous studies, scientists have observed TCE biodegradation performance in varied temperature circumstances, where the chlorinated solvent bioremediation increases with temperature above room temperature [25]. In addition, Bacillus proteolyticus has been reported to produce a significant amount of EPS for survival in contaminated environments by encapsulating the cells and protecting them from direct contact with contaminants [26]. Additionally, EPS facilitates the remediation of contaminants through mechanisms such as flocculation, emulsification, and the immobilization of pollutants [27]. Depending on the type of microorganisms involved, the optimal temperature for TCE dechlorination in contaminated soil and groundwater was found to be effective between 20 and 38 °C [5]. This temperature range supports microbial activity and enhances enzymatic processes involved in TCE degradation, thereby facilitating more efficient remediation strategies.
Therefore, this research finding unveiled the significant potential of Bacillus proteolyticus SAN8, a facultative anaerobe from the San Marcos River sediment, for the remediation of TCE both under aerobic and anaerobic conditions. Its metabolic flexibility enables this bacterium to thrive in different environmental conditions, making it a great candidate for the remediation of sediment and industrial wastewater contaminated with chlorinated solvents, including TCE. Initial studies proved that Bacillus proteolyticus SAN8 has the potential for degrading TCE in different environments; however, more extensive research is required to understand its mechanisms and assess its long-term efficacy in field studies. This work may lead to the development of better strategies for dealing with TCE pollution in any type of environment where it occurs. Nevertheless, the detailed biotransformation pathways and byproducts of TCE degradation will be analyzed in future studies to consider their overall toxicity.

4. Conclusions

The sediment of the San Marcos River hosts TCE-degrading bacteria capable of degrading TCE under both aerobic and facultatively anaerobic conditions. Among the twelve isolated bacteria, Bacillus proteolyticus SAN8 emerged as the most effective TCE degrader. At pH 7, a temperature of 30 °C, and TCE concentrations of 40 mg/L, 80 mg/L, and 120 mg/L, Bacillus proteolyticus SAN8 achieved TCE degradation of 91.20%, 82.33%, and 69.12%, respectively, within 5 days. The higher concentrations of TCE and the elevated incubation temperature contributed to increased cell biomass, likely facilitated by enhanced production of cell-bound EPS. Therefore, bacteria isolated from contaminated environments serve as valuable microbial resources for effective TCE biodegradation.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/w16202941/s1: Figure S1: Screening of the river sediment bacteria for TCE degradation at a concentration of 40 mg/L at 25 °C in 5 days; Figure S2: Phylogenetic position of San Marcos River bacteria. (a). Aeromonas sp. SAN1; (b). Bacillus sp. SAN2; (c). Gordonia sp. SAN3.

Author Contributions

Conceptualization, R.G. and S.H.; methodology, R.G.; software, R.G.; validation, R.G., S.H. and C.J.; formal analysis, C.J.; investigation, R.G.; resources, S.H.; data curation, C.J.; writing—original draft preparation, R.G.; writing—review and editing, S.H.; visualization, R.G.; supervision, S.H.; project administration, S.H.; funding acquisition, S.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Department of Energy’s Minority Serving Institution Partnership Program (MSIPP) managed by the Savannah River National Laboratory under BSRA contracts TOA603635 and TOA655810.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy reasons.

Acknowledgments

The authors would like to thank Texas State University, TX, USA, and UPES Dehradun, India, for their support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. (a) Screening of the river sediment bacteria for TCE degradation at a TCE concentration of 80 mg/L at 25 °C for 5 days. (b) Phylogenetic position of Bacillus proteolyticus SAN8.
Figure 1. (a) Screening of the river sediment bacteria for TCE degradation at a TCE concentration of 80 mg/L at 25 °C for 5 days. (b) Phylogenetic position of Bacillus proteolyticus SAN8.
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Figure 2. Time-dependent TCE degradation by Bacillus proteolyticus SAN8 at the TCE concentration of 80 mg/L and temperature of 25 °C.
Figure 2. Time-dependent TCE degradation by Bacillus proteolyticus SAN8 at the TCE concentration of 80 mg/L and temperature of 25 °C.
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Figure 3. Effect of pH (6–8) on TCE degradation and DCE of Bacillus proteolyticus SAN8 at TCE concentration of 80 mg/L, temperature of 25 °C, and incubation time of 5 days.
Figure 3. Effect of pH (6–8) on TCE degradation and DCE of Bacillus proteolyticus SAN8 at TCE concentration of 80 mg/L, temperature of 25 °C, and incubation time of 5 days.
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Figure 4. Effect of TCE concentration (40–120 mg/L) and temperature on Bacillus proteolyticus SAN8 TCE degradation and dry cell weight (DCW), at temperatures of (a) 25 °C and (b) 30 °C.
Figure 4. Effect of TCE concentration (40–120 mg/L) and temperature on Bacillus proteolyticus SAN8 TCE degradation and dry cell weight (DCW), at temperatures of (a) 25 °C and (b) 30 °C.
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Gurav, R.; Ji, C.; Hwang, S. Investigating the Potential of River Sediment Bacteria for Trichloroethylene Bioremediation. Water 2024, 16, 2941. https://doi.org/10.3390/w16202941

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Gurav R, Ji C, Hwang S. Investigating the Potential of River Sediment Bacteria for Trichloroethylene Bioremediation. Water. 2024; 16(20):2941. https://doi.org/10.3390/w16202941

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Gurav, Ranjit, Chang Ji, and Sangchul Hwang. 2024. "Investigating the Potential of River Sediment Bacteria for Trichloroethylene Bioremediation" Water 16, no. 20: 2941. https://doi.org/10.3390/w16202941

APA Style

Gurav, R., Ji, C., & Hwang, S. (2024). Investigating the Potential of River Sediment Bacteria for Trichloroethylene Bioremediation. Water, 16(20), 2941. https://doi.org/10.3390/w16202941

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