SUSTAINABLE BIOREMEDIATION

Environmental pollution with petroleum hydrocarbons is the most severe issue primarily for large resource-producing regions. The growth in oil production and refining is accompanied by the increased scale and volume of oil pollution due to accidental oil spills and generated waste, leading to an increased environmental threat, reduction in agricultural land, a decline in soil fertility and ill-health. Nature is negatively affected by the areas used for long-term storage of solid and liquid oil-containing waste associated with the emission of volatiles and migration of petroleum products and related metals into the adjacent landscape.

In contaminated soils the self-cleaning processes can occur from several months to several decades depending on the level of contamination, soil characteristics, climatic conditions, and a number of other factors. Due to significant disadvantages, such as high costs and additional negative impacts on ecosystems, the use of mechanical, thermal, and physicochemical methods to clean up polluted ecosystems has reached the limits [1]. Technologies of biological remediation of oil-polluted soils become increasingly important and widely used as they are eco-friendly and quite efficient, resulting in complete mineralization of hydrocarbon pollutants (hydrocarbons), and economically profitable.

Petroleum hydrocarbons are a common cause of soil contamination through spillages, leaking tanks/pipelines and other industrial activities. Bioremediation of petroleum hydrocarbon contaminated soil may be conducted either in-situ, or ex-situ following excavation for treatment typically in biopiles or windrows. The least intensive form of bioremediation is intrinsic bioremediation where naturally occurring microorganisms have the capability and suitable environmental conditions to allow degradation of the contamination. The progress of bioremediation is monitored through sampling and analysis of the contaminants of concern e.g. total petroleum hydrocarbons or polycyclic aromatic hydrocarbons (PAHs) to reach the targeted level of treatment. Enhanced bioremediation is a common practice where soil condition is poorly suited to support growth of a hydrocarbon degrading microbial population. Additional nutrients, such as nitrogen and phosphorous, are applied (biostimulation) and in some cases additional microorganisms (bioaugmentation) in order to enhance the rate or completeness of contaminant removal.

Bioremediation is generally considered a more sustainable remediation approach to managing petroleum hydrocarbon contaminated soils than alternatives such as excavation and disposal to landfill or energy intensive thermal desorption [2, 3]. Incorporating wider sustainability issues into remediation projects was started in the 1990s by professional bodies such as the Network for Industrially Contaminated Land in Europe (NICOLE) and Contaminated Land: Applications in Real Environments (CLAIRE) in the UK [4]. A key white paper on how sustainable principles could be applied to remediation projects was produced by the Sustainable Remediation Forum (SURF), formed in the United States during 2006 [5]. SURF adopted a broad definition of sustainable remediation as being “a remedy or combination of remedies whose net benefit on human health and the environment is maximized through the judicious use of limited resources”. The key principles of sustainable remediation produced by SURF are shown in Fig. 1.

Fig. 1.
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Key principles of sustainable remediation and sustainable development.

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One of the key resources used in soil bioremediation are nutrients, principally nitrogen and phosphorous, added to promote growth of the hydrocarbon degrading microbial population. Inorganic fertilisers, such as those commonly used in agriculture, are commonly applied during bioremediation. However, inorganic fertilisers are associated with many negative environmental impacts including energy intensive production (nitrogen), large scale mining (phosphorous) and emissions from transportation. Using waste organic nutrients rather than synthetic fertilisers for soil bioremediation may therefore be a key consideration when adopting a more sustainable approach [6].

There are numerous examples of studies that have demonstrated the efficacy of using organic nutrients for bioremediation of soils contaminated by a range of petroleum hydrocarbons (Table 1). In addition to providing relatively slow-release nitrogen and phosphorous, organic wastes also serve as an additional source of organic matter and inoculum of hydrocarbon degrading microorganisms. Geilnik et al. [7] recently reported that increased degradation of petroleum hydrocarbons in soil amended with anaerobically digested sewage sludge (digestate) was linked to an increase in the percentage of alkB genes. In that study, the addition of digestate resulted in more diverse microbial communities than soils amended with mineral nutrients. Increase in the ratio of alkB genes was associated with the direct entry of these genes from the digestate, but also with the stimulation of digestate as a fertilizer and a source of nutrients for the indigenous microflora.

Table 1.   Examples of waste organic nutrient use in soil bioremediation
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The addition of substantial extra organic material into petroleum hydrocarbon contaminated soil could be considered to risk reducing contaminant bioavailability due to sorption onto organic matter. However, evidence from several studies suggests this effect is time limited and amendments such as compost enhance bioavailability of PAHs during the bioremediation process over time [8]. An additional benefit of organic amendments is the improvement in water holding capacity and retention that can reduce the need for watering [9].

Collection, handling, storage and processing of organic wastes requires careful management to prevent them being a significant source of environmental pollution. For example, it has long been recognised that runoff from animal waste/manures can cause significant pollution of groundwater and surface waters through eutrophication, depletion of oxygen from a high biochemical oxygen demand (BOD) and introduction of faecal pathogens [22].

In many countries, particularly those in the European Union, legislation has resulted in the amount of biodegradable waste being disposed of to landfill declining steadily since the turn of the century. Some of the wastes being diverted such as green waste and food waste collected from households are likely to be processed by composting or anaerobic digestion. Some materials such as composted fractions of residual organics arising from mechanical treatment of municipal solid waste (MSW) are more likely to contain contamination from a wide range of wastes disposed of by consumers e.g. batteries. These are less attractive as sources of alternative nutrients due to the high levels of contamination and are sometimes referred to as compost-like organics (CLO) to differentiate them from quality composts arising from source segregated materials like green waste and food waste. Such CLO materials are typically restricted by legislation to use as landfill capping layers.

The spreading of organic wastes on land has often been a controversial practice as it could be perceived as a disposal method avoiding the cost of landfilling or otherwise treating organic wastes. Land application of certain organic wastes such as municipal sewage sludge, especially from urban and industrialised areas, is frequently controlled by regulations with the strictest limits being where the application is to agricultural land. Heavy metals such as Cd, As, Cr, and Pb and a wide range of potential organic contaminants may be introduced to soils along with the beneficial nutrients and organic matter.

Certain organic wastes have themselves proven to be useful in reducing the bioavailability of soil metal contamination. For example, HuangFu et al. [23], developed a combination of dried waste animal blood from slaughterhouses and waste orange peel as a soil amendment for immobilisation of Cd. Interestingly, although Cd has been recognised for decades as a contaminant of concern in sewage sludge applied to land, mineral phosphate fertilisers are also a source of Cd and the long-term accumulation of Cd in soils is of sufficient concern to have generated considerable debate on how to regulate Cd input to soils from mineral phosphate fertilisers [24]. Improving soil quality through bioremediation using organic wastes instead of inorganic fertilisers is generally considered as a regenerative practice that is inherently more sustainable and also provides ecologically better outcomes with remediated soils having improved structure and organic matter content [25].

SYMBIOSIS BETWEEN SUSTAINABLE BIOREMEDIATION AND ORGANIC WASTE MANAGEMENT

The concept of symbiosis is a familiar one to biologists and ecologists and in those contexts the term refers to close relationships between organisms that are mutualistic and may be commensal or even parasitic. Industrial symbiosis describes using surplus resources from one commercial or industrial process in a beneficial way in another process. In the context of sustainable bioremediation and organic waste management, this symbiosis will normally be mutually beneficial as there is often a cost to managing or disposing of surplus materials such as organic wastes and a cost to purchasing the alternative that they can replace such as mineral fertiliser.

One of the most frequently cited locations where industrial symbiosis has been put into widespread practice for the longest time is the Kalundborg Eco-Industrial Park in Denmark. This developed around a power station, refinery and other industries, originating around 1959 and continuing to the present day. Kalundborg provides an early example of the use of organic nutrients in soil remediation. In 1999, Danish company A/S Bioteknisk Jordens used municipal sewage sludge from Kalundborg as a nutrient for bioremediation of contaminated soil [26].

Although such a symbiotic approach may appear to be common sense, the policies and strategies supporting a more ecosystems-based approach to dealing with wastes and restoring land are complicated and consider the challenges and most desirable outcomes from many different perspectives (Fig. 2).

Fig. 2.
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Sustainable bioremediation in the wider policy context.

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Modern waste management practices have for many years had an increasing focus on realising the value of materials by focusing on resource recovery. As a result of this, many organic wastes are now considered as valuable resources, particular in the context of one of the most prevalent of the modern environmental, economic and social concepts, the circular economy [27, 28]. The circular economy may be considered as a condition for achieving sustainability according to the definitions below [29]. The Circular Economy is “a regenerative system in which resource input and waste, emission, and energy leakage are minimised by slowing, closing, and narrowing material and energy loops. This can be achieved through long-lasting design, maintenance, repair, reuse, remanufacturing, refurbishing, and recycling.” Sustainability is “the balanced integration of economic performance, social inclusiveness, and environmental resilience, to the benefit of current and future generations.”

Also of relevance is the bioeconomy or biobased economy concept. This is based on producing renewable biomass and converting this and various waste streams into food, energy and bioproducts e.g. bio-composites, bio-plastics. Calicioglu and Bogdanski [30] provide a useful definition of the bioeconomy as being: “the production, utilization and conservation of biological resources, including related knowledge, science, technology, and innovation, to provide information, products, processes and services across all economic sectors aiming toward a sustainable economy.”

Gillespie and Philp [2] consider bioremediation as an attractive technology that is integral to the bioeconomy and to achieving the goals of greater sustainability. They also emphasise importance of bioremediation to wider bioeconomy strategies as healthy soils are also needed to grow non-food e.g. biomass crops for the bioeconomy and that healthy soils play a key role in capturing around 20% of man-made carbon dioxide emissions.

There are a range of opportunities for industrial symbiosis between sustainable bioremediation and organic waste management within the frameworks of circular economy, bioeconomy and sustainability. Organic wastes can be directly applied to contaminated soils, composted prior to mixing with contaminated soils or untreated materials can be mixed with contaminated soils and both composted together, a process generally termed co-composting [31]. Anaerobic digestion of organic wastes has the advantage of generating renewable energy from biogas before the digestate is used in bioremediation.

The development of long-term strategies along with co-ordination on regional scales is required to accelerate the use of locally available organic wastes as part of sustainable bioremediation of contaminated sites. Waste processors need to have guaranteed outlets for processed wastes and there may be an opportunity to producing bespoke bioremediation amendments from a combination of different wastes to match the specific requirements of remediation projects depending on soil types and types of contamination. There is a potential win-win scenario with waste processors generating a new revenue stream or saving on disposal costs and remediation practitioners sourcing cost effective organic amendments tailored to their needs. Co-location of organic waste processing with bioremediation in an integrated facility can be envisaged. This could be cost effective for smaller contaminated sites where excavated contaminated soils are brought to such a facility and exchanged for previously remediated clean soils. Emissions from haulage of soils to and from such a site would need to be incorporated into the assessment of the overall sustainability of any remediation project.

Sustainable bioremediation recognises the need to consider the wider impacts that the remediation process itself may have on the environment and human health with a focus on the net benefit. An important factor to consider when using organic nutrients such as animal manures and sewage sludge is that they frequently contain antibiotic residues, antibiotic resistant bacteria and resistance genes. The need to consider potential risks of enriching antimicrobial resistant bacteria through applying such nutrients to contaminated soils has only recently started to be explored [32]. Microbial populations in contaminated soils are under selection pressure from organic e.g. hydrocarbons and inorganic e.g. heavy metal contaminants and the co-selection of resistance to antibiotics and contaminants drives greater antimicrobial resistance traits. The significance of the risk of horizontal gene transfer between soil microorganisms to human commensal or pathogenic bacteria needs to be better understood. For example, multi-resistant indigenous strains of Pseudomonas aeruginosa closely related to isolates of clinical significance to patients suffering from cystic fibrosis have been identified in hydrocarbon contaminated soils [33].

The antimicrobial resistance issue should be considered in the context of sustainable remediation given the focus on the net benefit to human health and the environment. The seriousness of the growing global threat to human health from antimicrobial resistance cannot be underestimated. A recent UK government report has estimated that global deaths from antimicrobial resistance could rise from 700,000 to 10 million per year by 2050 unless strong policies are in place to prevent this [34]. Understanding and quantifying the potential risks to human health from adding organic nutrients containing antibiotic residues, antimicrobial resistant bacteria and genes to contaminated soils already enriched with antimicrobial resistant strains is an important area for future research.

Composting may offer a solution to reducing risks from antibiotics and resistant bacteria when using organic wastes such as animal manures and sewage sludges in bioremediation. The aerobic composting process has been shown to degrade antibiotics in poultry litter [35] and reduce the abundance of antibiotic resistance genes in composted cattle manure [36]. A recent and comprehensive review of composting as bioremediation showed a wide range of starting concentrations of total petroleum hydrocarbons up to 380,000 mg kg–1 have been successfully treated with removal efficiencies up to 99% in many different soil types [37]. One potential disadvantage of composting as a bioremediation treatment is if the contamination e.g. TPH or PAHs fails to reach an acceptable level then a larger volume of contaminated soil will require further treatment or disposal.

CONCLUSIONS

Sustainable remediation considers a net benefit to human health and the environment from remediation processes. The application of sustainable bioremediation can be viewed as contributing to the circular economy and bioeconomy and in turn to wider sustainability. A greater net benefit to human health and the environment may be achieved through better integration of bioremediation with organic waste management practices. In the context of a circular economy and bioeconomy, organic waste management is moving towards greater recognition of the nutrient value of organic wastes. Raw or composted organic wastes may be used in place of synthetic fertilisers during bioremediation or organic wastes added to contaminated soils for co-composting as the form of bioremediation.

In addition to the potential risks arising from the presence of organic and inorganic chemical contaminants or pathogenic microorganisms, the use of some organic wastes such as animal manures and sewage sludge carry potential risks of enhancing the number and diversity of antibiotic resistant bacteria in contaminated soils. There are plausible pathways for human infection with resistant commensal and/or pathogenic strains to occur from environmental exposure. Composting of organic nutrients has potential to reduce some of these risks. Although there is a clear potential for greater symbiosis between sustainable bioremediation of hydrocarbon contaminated soils and the management of organic wastes, further research is required to improve the processes and manage potential risks.