Abstract
The ability of microorganisms to transform pollutants is well documented. However, in many cases microbial communities with the desired capabilities may develop too slowly or may not be sustained. In these cases, manipulation of the microbial composition may be advantageous. Bioremediation has been established as an environmental friendly treatment capable of improving the removal of the contaminants in natural and environmentally systems by circumventing insufficient response time and initiating the removal with a minimal lag phase. Bioremediation exploits the microbial ability to transform contaminants into less harmful compounds. Bioremediation techniques encompass natural attenuation, biostimulation, and bioaugmentation. While natural attenuation and biostimulation by indigenous microorganisms might work for certain applications, bioaugmentation using microbial populations with specialized capabilities for degrading the contaminants is often advantageous, and will be the focus of this chapter.
Bioaugmentation has been widely applied to assist bioremediation, but it has also frequently been associated with significant challenges and limited success, which is most likely due to lack of information leading to inappropriate application strategies.
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Keywords
- Bioaugmentation
- Delivery limitations
- Immobilization of bioaugmentation strains
- Survival of bioaugmentation strains
1 Introduction
Bioaugmentation works by manipulating the genetic composition in order to improve the biodegradation capability. This can be accomplished through amendment of specialized microbial strains or enriched microbial consortia. The inoculated cells may be directly responsible for the degradation of the pollutant or work indirectly by supplying the indigenous population with partial degradation or important metabolites for increased activity. Understanding of these scenarios relative to non-bioaugmented controls has resulted in limited well-characterized field applications. Numerous laboratory- and demonstration-scale applications have been described and reviewed [e.g., 1]. In this chapter we will describe frequent occurring challenges associated with bioaugmentation and possible solutions.
2 Delivery Limitations in Heterogeneous Soils
The nature and physical conditions of the contaminated environment might complicate the application of bioaugmentation. Contaminated groundwater in subsurface soil and similar porous matrices with high levels of heterogeneity pose challenges to distribution of augmented materials, whereas aqueous environments allow for better mixing and distribution of the amended cultures. Amendments to subsurface soils are usually mediated by pumping bacterial suspensions into the groundwater. Silted and clay soils with low pore size might require significant pressure to ensure a proper distribution with cells reaching microfractures and interstitial pore water. However, extensive pressure could result in cell lysis and might pose a large problem for the successful bioremediation performance.
An efficient full-scale delivery system in subsurface saturated soils employs biocurtains or permeable reactive barriers in which a row of strategically placed and closely spaced injection wells are installed in the path of the pollution plume migration [e.g., 2]. The natural flow of contaminated groundwater passes through the biocurtain, reducing the need for hydraulic controls or bioaugmentation over a large spatial area. To ensure remediation success, careful system monitoring partnered with time for system “rest” to account for diffusion limitations.
3 Parameters Limiting the Survival of Bioaugmented Bacteria
The ability of bioaugmentation cultures to survive and function over time depends on a complex interaction of multiple variables. Among the variables receiving current attention are attachment to surfaces and substrate availability.
A bacterial culture’s ability to incorporate into a biofilm or to attach to a solid surface can improve survival by offering protection from harsh chemical conditions in the environment, from loss due to grazing by protozoa, and from washout when growth rates are slower than hydraulic retention times. These phenomena have been studied predominately in reactor systems, but are of universal importance for all bioaugmentation applications. A common bioaugmentation approach involves amendment of bacterial suspensions as planktonic cells. The bulk of the cells may have difficulty adsorbing to surfaces and are thus subject to washout and protozoan grazing activity. In fact, many protozoa specifically prey on laboratory culture strains used for bioaugmentation [3, 4]. Amendment together with selective inhibitory compounds such as nystatin and cycloheximide targeting rotifers and other protozoa can effectively reduce protozoan activity [5]. However, it still remains to be demonstrated that concomitant amendment of protozoan inhibitory compounds is economically feasible on a larger scale. An alternative is to choose microorganisms capable of adsorbing to surfaces or even producing protective biofilms and thereby become inaccessible for the protozoa. Several attempts have therefore been made to improve adsorption by immobilization of the augmentation cultures, for example, by introducing a starvation period prior to augmentation to enhance cell surface hydrophobicity [e.g., 6]. Additionally, amendment of microorganisms grown as self-forming dense aggregates (granules) may improve survival. Growth in granules results in compact microbial structures with increased resistance to toxins, reduced grazing activity and, when operated with a settling step, promotes a hydraulic selection pressure supporting long-term survival in suspended systems [e.g., 7]. In aqueous systems, implementation of membrane bioreactors (MBR) might withhold the bioaugmented cells and eliminate wash out effects of planktonic cells [8]. Augmentation of aggregated consortia or cells added simultaneous with the addition of nutrients has been shown to improve the growth and activity of the microbes [9].
Immobilization improves the longevity of the process [10] as it allows the cells to settle and buffer the augmented cells against suboptimal environmental conditions, protozoa, competing indigenous microbes and viruses [4]. Immobilization of the augmentation cultures can be obtained by mixing with various carriers such as porous materials (e.g., gel beads, lignite, isolite, and charcoal) or by encapsulation in gel matrices such as agar, alginate, or polyurethane [e.g., 11]. The capsule matrix can be combined with addition of electron donors and acceptors, as well as surfactants and nutrients to improve initiating activity. Maintaining a hydrophobic cellular surface during the isolation may also improve attachment of the cells to various surfaces and thereby reduced washout [12]. Several studies have suggested that microorganisms deriving from the same ecological niche as the polluted area have better chances of surviving in the environment after augmentation [e.g., 13, 14]. This hypothesis is substantiated by the species-dependent survival among various augmentation strains observed in multiple studies [e.g., 15], and stress the importance of knowing the augmentation strains as well as the ecological niche. See Table 1 for delivery methods associated with bioaugmentation.
Loss of activity due to insufficient substrate availability also constitutes a problem, especially since most bioaugmentation cultures derive from highly artificial laboratory environments with high substrate availabilities. Application of bioaugmentation strains with zymogenous or low substrate affinities (high K m) such as r-strategists with fast substrate turnover (high V max) is an important feature for good augmentation cells [21]. Furthermore, the ability to rapidly shift between dormancy and active stages supports the selection of a successful bioaugmentation culture. The bacteria must be able to degrade the contaminant with favorable kinetics in order to result in high removal efficiencies. Augmentation cultures should be able to maintain the ability to degrade the pollutant of interest even after periods without exposure to contaminants, which could occur periodically during growth prior to or after augmentation. Augmentation cultures should also be able to grow using readily available carbon sources while maintaining the ability to degrade the pollutant [22].
Genetic modification can enhance a cell’s ability to degrade contaminants. However, genetic modified organisms are susceptible to lose the genetic elements coding for the degradation ability especially when present in mobile genetic units such as plasmids. In fact, only very few examples of amendment of such modified organisms have turned out to perform better than natural and non-modified organisms (reviewed by Cases and de Lorenzo [23]). Legal regulations on releasing genetically modified organisms to the environment can limit their use. However, loss of the augmented bacteria due to the lack of knowledge about microbial ecophysiology is an even larger barrier for application [23]. Lack of long-term survival often requires regular resupplementation, but improved understanding of the factors influencing longevity and adaptations to an ecosystem may lead to future improvements. Further study into the survival of genetically modified organisms has been initiated [1], and it has been hypothesized that a few strains possess exceptional catabolic and survival abilities which makes them better suited for bioaugmentation [24]. These microorganisms, also denoted as Heirloom superbugs, have evolved over years in laboratory transformations and possess high resistance properties and can easily be cultivated. Experiences from full-scale applications still remain to be explored.
4 Documenting Bioaugmentation Performance
Following bioaugmentation, the removal of the contaminant should be accompanied by measuring the presence and activity of the amended cells. It has been proposed to follow amendment by labeling cells by staining or gfp-labeling. This allows visual tracking of the strain in the given environment [e.g., 25, 26]. Other studies of the survival of non-native strains have typically applied qPCR or RT-(q)PCR targeting phylogenetic or functional markers [e.g., 27–29].
A more sophisticated approach to monitor the survival and activity of individual bioaugmentation strains has been demonstrated through a case study on degradation of aromatic hydrocarbons in activated sludge using Pseudomonas monteilii [26]. This multiphasic approach involved genome sequencing to establish highly specific qPCR and RT-qPCR tools for in situ cell enumerations and quantifications of transcripts from functional genes, stable isotope probing to follow growth on the amended target compounds, and gfp-tagging to visualize the cells directly in the sample. The study revealed that the planktonic cells were quickly washed out and only a minor part (3%) of the added cells were present after a few days. However, the remaining cells continued to actively degrade the aromatic hydrocarbons and to actively incorporate carbon into its biomass.
5 Interactions with Host Community
Bioaugmentation performance is frequently impaired by the lack of knowledge about the indigenous microbial populations and about the microbe’s ability to survive in the new ecosystem. Instead, most studies have focused on the ability of the augmentation culture to degrade specific contaminants with less attention to phenotypic properties that might improve its adaptation. Understanding the composition of the indigenous communities and how these might interact with the augmented strain will most likely provide important knowledge to further improve their survival. Empirical knowledge on the competitiveness of the amended strain relative to the receiving environment might therefore reveal which strains have greater survival abilities. Choosing the best strains should be based on both the ability to interact and survive in the environment as well as the ability to degrade specific pollutants.
6 Bioaugmentation Applications Beyond Soil and Groundwater Remediation
While bioaugmentation is mostly associated as a bioremediation strategy, it is also applicable to many other fields of environmental biotechnology. Examples of recent bioaugmentation studies shown in Table 2 reveal the wide range of current applications. Much of the recent work has focused on improved biological treatment of industrial wastewater and municipal wastewater. Industrial wastewater has its own set of treatment challenges including high organic loadings, salinity, pH, recalcitrance, and color. Here, similar to approaches used for bioremediation, bioaugmented microorganisms are isolated (or consortia are enriched) with highly specific metabolisms. The targeted contaminants can be similar to contaminants bioremediated in soil or groundwater (e.g., naphthalene [8]), but can also be highly specific to the industry producing the waste (e.g., tetrahydrofuran [36]; tannery waste [37]; pharmaceutical wastewater [38], and tobacco wastewater [39]). An important difference for industrial wastewater is that treatment generally occurs in engineered reactor systems rather than in the subsurface. However, an interesting recent development has been the use of constructed wetlands for industrial wastewater treatment. Readers are referred to the recent review on use of constructed wetlands for industrial wastewater treatment for a discussion on the role of bioaugmentation in these systems [40].
Bioaugmentation efforts for domestic municipal wastewater have focused on enhancing start-up. Because the function of the community is less specialized (i.e., removal of chemical oxygen demand and nitrogen species can be mediated by a wider range of bacteria) the approach has differed from other areas of bioaugmentation. Overcoming the challenges of start-up in cold climates, which have the particular challenges of temperature-related slower metabolic reactions, has been approached both by using cold-adapted consortia enriched for nitrogen oxidizing activity [31] and using bacterial strains isolated from cold habitats [30].
A less-studied application of bioaugmentation for improved domestic municipal wastewater treatment has focused on the emerging issue of trace-level organic compounds (TOrCs) removal. Several unique challenges exist for this treatment process. Unlike industrial wastewater treatment, bacterial degradation activity must occur at extremely low contaminant concentrations and unlike in bioremediation in soils and groundwater, the bacteria must be able to degrade the contaminants while in a nutrient-rich habitat and in the presence of high concentrations of readily available substrates. Many bacteria have been identified with capabilities for degrading TOrCs in isolation [e.g., 41–44]. However, most have not been tested for their suitability to the conditions encountered in municipal wastewater secondary treatment. In the study by Zhou and coworkers [22] isolated bacteria were specifically targeted for their applicability to degrade TOrCs in the complex wastewater treatment habitat. Modeling suggests that routine small bioaugmentation doses have high potential for mitigating impacts from this emerging contaminant class [32].
Biogas production during anaerobic digestion is another area that has benefited from bioaugmentation. The complexity of community interactions of anaerobic communities [45], sensitivity of anaerobic digestion to perturbation [e.g., 46], and known influence of community structure on system performance [e.g., 47] make these systems ideal for bioaugmentation. Multiple examples of bioaugmentation for the initial transformation of cellulosic/lignocellulosic substrates, with a fungus [48], a Clostridium sp. [49], a proprietary cellulolytic bioculture [50], and a mixture of hydrolytic bacteria [51], demonstrate the potential for use of bioaugmentation to increase availability of feedstocks often considered recalcitrant in anaerobic digestion. Bioaugmentation also holds promise for overcoming ammonia inhibition – a common complication during anaerobic digestion – through addition of ammonia-oxidizing Clostridium sp. [52]. These reports suggest that with further study many of the complications associated with anaerobic digestion and biogas production could be tackled through use of bioaugmentation.
The challenges of bioaugmentation are often unique to the targeted habitat and treatment goal. For some bioaugmentation applications it is not necessary to sustain a stable culture in the system, and instead, it is sufficient to use pulse-dosing in response to dynamic conditions, e.g., in water treatment with irregular loadings. In such environments it is important that augmentation is followed by high activity to overcome temporal accumulations or periods with high loadings. However, in most other applications selection of the right organism for the environment is pivotal for successful bioaugmentation. Application of highly specific and sensitive molecular tools to detect and measure the performance of various strains in the environment is a critical research need and will improve our understanding of bacterial survival and adaptation. In the future, these tools, along with mathematical modeling, will provide a platform to improve the assessment of the augmentation performance and bacterial survival resulting in a wider range of bioaugmentation applications.
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Gough, H.L., Nielsen, J.L. (2016). Bioaugmentation. In: McGenity, T., Timmis, K., Nogales, B. (eds) Hydrocarbon and Lipid Microbiology Protocols. Springer Protocols Handbooks. Springer, Berlin, Heidelberg. https://doi.org/10.1007/8623_2016_205
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DOI: https://doi.org/10.1007/8623_2016_205
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