Bio-electrokinetic remediation of crude oil contaminated soil enhanced by bacterial biosurfactant

https://doi.org/10.1016/j.jhazmat.2020.124061Get rights and content

Highlights

  • Biosurfactant (BS) produced by marine bacteria belongs to lipopeptide in nature.

  • Bacteria degraded the higher molecular weight hydrocarbon (C8 to C28) about 97%.

  • BS in electokinetic remediation (EK) enhanced the biodegradation rate than EK.

  • BS enhanced the solubilization of hydrocarbon and leads to faster electromigration.

  • BIO-EK combined with BS can be used to enhance bioremediation of polluted soils.

Abstract

The present study evaluating the coupling between bioremediation (BIO) and electrokinetic (EK) remediation of crude oil hydrocarbon by using bio-electrokinetic (BIO-EK) technique. The application of bacterial biosurfactant (BS) may increase the remediation efficiency by increasing the solubility of organic materials. In this work, the potential biosurfactant producing marine bacteria were isolated and identified by 16S rDNA analysis namely Bacillus subtilis AS2, Bacillus licheniformis AS3 and Bacillus velezensis AS4. Biodegradation efficiency of crude oil was found as 88%, 92% and 97% for strain AS2, AS3 and AS4 respectively, with the optimum temperature of 37 °C and pH 7. FTIR confirm the BS belongs to lipopeptide in nature. GCMS reveals that three isolates degraded the lower to higher molecular weight of the crude oil (C8 to C28) effectively. Results showed that use of BS in electokinetic remediation enhance the biodegradation rate of crude oil contaminated soil about 92% than EK (60%) in 2 days operation. BS enhances the solubilization of hydrocarbon and it leads to the faster electromigration of hydrocarbon to the anodic compartment, which was confirmed by the presence of higher total organic content than the EK. This study proven that the BIO-EK combined with BS can be used to enhance in situ bioremediation of petroleum contaminated soils.

Introduction

Large scale production of crude oil and its transportation leads to huge chances for oil spills in soil, and sea water environments (Nriagu, 2011). The major parts of crude oil are hydrocarbon with low and high molecular weights and they are accessible by many microorganisms including bacteria, fungi, yeast, and archaea (Varjani, 2017). The microorganisms involved in various complicated pathways in the biodegradation process by producing key molecules that are acting as synergistic intermediates to enhance the biodegradation process in electrokinetics (Rajasekar and Ting, 2010; Li et al., 2012, Gill et al., 2014, Elumalai et al., 2017). Synthetic surfactants such as cetyltrimethyl ammonium bromide (cationic), sodium lauryl sulphate (anionic), phospholipids phosphatidyl serine have been widely used in the oil industry for oil spills clean-up process, enhanced oil recovery, but problem associated with these synthetic surfactants is their toxicity and non-biodegradability (Lima et al., 2011). Alternative options to overcome these problems are biosurfactant (Perfumo et al., 2010). Biosurfactants are surface-active molecules produced by fungi, bacteria and yeast and produced mostly as extracellular products during the microbe’s growth in starvations and hyper environments including pH, temperatures and nutrient depletions (Naeem and Qazi, 2019). The biosurfactant can be classified into several types including lipopeptides, phospholipids, glycolipids, natural lipids, lipopolysaccharide, and fatty acids.

Biosurfactant is having numerous advantages like environmentally friendly, biodegradable, stable at higher temperature and pH, can be synthesized using inexpensive raw material and non-hazardous (Virkutyte and Varma, 2011). This feature makes cheap and simple production of biosurfactant with industrial and agricultural waste substrates and in turn which reduces waste and contaminants indirectly (Campos et al., 2013, Parthipan et al., 2017a, Parthipan et al., 2018a, Parthipan et al., 2018b, Tan and Li, 2018). Biosurfactant having an aptitude to accrued at the interface of two immiscible liquids or between a liquid or solid (Sadouk et al., 2008). By reducing the surface and interfacial tension, they dropping the repulsive forces among two different stages and permit them to blend and intermingle more simply (Patowary et al., 2017). Thermophilic structure of biosurfactant increases the surface area of hydrophobic water-insoluble substances and increases bio-availability, which will assist in biodegradation by microorganisms (Parthipan et al., 2018a). These surface activities make surfactant as excellent emulsifiers, foaming, and dispersing agents (Lim et al., 2009).

Electrokinetics (EK) is a method to separate the heavy metals in solid waste or solid matter (Rajasekar et al., 2010, Huang et al., 2018). Limited direct current (DC) is applied to electrodes and extraction of metals based on the charges. EK removal of a pollutant has established as a potential approach for cleaning up heavy metal polluted soils (Khalid et al., 2017). The outcome of the electrokinetic remediation is to effective separation of molecules based on electroosmosis, electromigration, and electrophoresis (Park et al., 2010). In addition to physical and biological factors, electrochemical factors are having a key impact on the bioremediation rates (Agu and Okoli, 2014). The efficacy of Eh measurements, Eh-pH illustrations, and galvanic relations in bioremediation reactions have been well recognized (Verma and Kuila, 2019). The sluggishness of the bio-oxidation process and the real-time application problems related to the collecting of adequate levels of the biomass of the microorganisms have habitually restricted the scope and broader application of bioremediation (Chandra and Chowdhary, 2015). It has been revealed that the cell biomass of specific stains and their activity might be improved the electrochemical reactions. The electro-bioremediation technique has the advantage of being able to simultaneously increasing the degradation rates and cell yield in the hydrocarbon polluted environment (Koshlaf and Ball, 2017, Verma and Kuila, 2019).

In this work, we have collected the seawater sample from mangroves for the isolation of biosurfactant synthesizing bacterial species. Isolated marine bacterial strains were identified by 16S RNA gene sequencing. All the isolated strains are screened for biosurfactant production and subjected to optimization of biosurfactant production by alteration of pH and temperature. Extracted biosurfactant were analysed using gas chromatography and mass spectrometry (GC-MS) and Fourier transform infrared spectroscopy (FT-IR) analysis. Further, the purified biosurfactant was applied for biodegradation of crude oil by using bio-electrokinetic approach.

Section snippets

Sample collection

The seawater sample was collected from mangroves forest at Pichavaram, Tamil Nadu, India (latitude-11.4319° N and longitude-79.7810° E (Fig. S1). Sample was collected using sterile sample containers and kept in an icebox and immediately transported to lab.

Isolation and identification of bacterial strains

For isolation of marine bacteria from seawater samples, the standard serial dilution method and pour plate technique were employed by using zobell marine medium (Hi-media, India) for this isolation of bacteria and the inoculated plates were

Isolation and identification of marine bacteria

The seawater sample was used to isolate marine bacterial strains with the crude oil-degrading ability. About seven dissimilar colonies were isolated and pure strains are used for the biosurfactant screening. Based on the preliminary screening three bacterial strains are selected as efficient biosurfactant producers among the bacterial strains. Biochemical characterization revealed that all the isolated bacterial strains are Gram-positive and also belongs to Bacillus species (Table S1). For the

Conclusions

In the present study, we have identified three potential bacterial strains from seawater associated with mangroves trees. All three bacterial strains are showed significant biosurfactant production capability. Growth conditions including pH and temperature are optimized and found that pH 7.0 and temperature 40 ºC are optimum for all three strains. FT-IR and GC-MS analysis confirm that extracted biosurfactant are lipopeptide in nature with higher emulsification activity. The Electrokinetic

CRediT authorship contribution statement

Arumugam Arul Prakash: Experimental work, Field collection, Writing - original draft. Nataraj Srinivasa Prabhu: Methodology, Field collection. Punniyakotti Parthipan: Validation, Writing - review & editing. Mohamad S. AlSalhi: Resources, Funding acquisition, Writing - review & editing. Sandhanasamy Devanesan: Validation, Formal analysis, Writing - review & editing. Aruliah Rajasekar: Project administration, Supervision, Validation, Writing - review & editing. Muthusamy Govarthanan: Writing -

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.

Acknowledgements

The authors are grateful to the Deanship of Scientific Research, King Saud University, Kingdom of Saudi Arabia, for funding through Vice Deanship of Scientific Research Chairs.

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