Plasmid-Mediated Bioaugmentation for the Bioremediation of Contaminated Soils
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fmicb-08-01966 October 5, 2017 Time: 15:18 # 1 REVIEW published: 09 October 2017 doi: 10.3389/fmicb.2017.01966 Plasmid-Mediated Bioaugmentation for the Bioremediation of Contaminated Soils Carlos Garbisu1, Olatz Garaiyurrebaso2, Lur Epelde1, Elisabeth Grohmann3 and Itziar Alkorta1* 1 Soil Microbial Ecology Group, Department of Conservation of Natural Resources, Neiker Tecnalia, Derio, Spain, 2 Instituto Biofisika (UPV/EHU, CSIC), Department of Biochemistry and Molecular Biology, University of the Basque Country, Bilbao, Spain, 3 Beuth University of Applied Sciences, Berlin, Germany Bioaugmentation, or the inoculation of microorganisms (e.g., bacteria harboring the required catabolic genes) into soil to enhance the rate of contaminant degradation, has great potential for the bioremediation of soils contaminated with organic compounds. Regrettably, cell bioaugmentation frequently turns into an unsuccessful initiative, owing Edited by: to the rapid decrease of bacterial viability and abundance after inoculation, as well as Tatiana Venkova, University of Texas Medical Branch, the limited dispersal of the inoculated bacteria in the soil matrix. Genes that encode the United States degradation of organic compounds are often located on plasmids and, consequently, Reviewed by: they can be spread by horizontal gene transfer into well-established, ecologically Gloria Del Solar, competitive, indigenous bacterial populations. Plasmid-mediated bioaugmentation aims Consejo Superior de Investigaciones Científicas (CSIC), Spain to stimulate the spread of contaminant degradation genes among indigenous soil Spiros Nicolas Agathos, bacteria by the introduction of plasmids, located in donor cells, harboring such genes. Catholic University of Louvain, Belgium But the acquisition of plasmids by recipient cells can affect the host’s fitness, a crucial Fabián Lorenzo, aspect for the success of plasmid-mediated bioaugmentation. Besides, environmental Universidad de La Laguna, Spain factors (e.g., soil moisture, temperature, organic matter content) can play important *Correspondence: roles for the transfer efficiency of catabolic plasmids, the expression of horizontally Itziar Alkorta [email protected] acquired genes and, finally, the contaminant degradation activity. For plasmid-mediated bioaugmentation to be reproducible, much more research is needed for a better Specialty section: selection of donor bacterial strains and accompanying plasmids, together with an in- This article was submitted to Evolutionary and Genomic depth understanding of indigenous soil bacterial populations and the environmental Microbiology, conditions that affect plasmid acquisition and the expression and functioning of the a section of the journal Frontiers in Microbiology catabolic genes of interest. Received: 20 May 2017 Keywords: biodegradation, catabolic plasmid, fitness cost, horizontal gene transfer, soil pollution Accepted: 25 September 2017 Published: 09 October 2017 Citation: INTRODUCTION Garbisu C, Garaiyurrebaso O, Epelde L, Grohmann E and Alkorta I Soils play a vital role in the provision of ecosystem services and harbor one of the most complex (2017) Plasmid-Mediated and diverse biological communities on Earth (Barrios, 2007). Therefore, the preservation of soil Bioaugmentation quality/soil health (both terms are often used interchangeably), defined as “the capacity of soil to for the Bioremediation of Contaminated Soils. perform its ecosystem processes and services, while maintaining ecosystem attributes of ecological Front. Microbiol. 8:1966. relevance” (Garbisu et al., 2011), is currently a matter of great priority. Contamination is one of the doi: 10.3389/fmicb.2017.01966 most important causes of soil degradation. Only in Europe, there are around 2.5 million potentially Frontiers in Microbiology| www.frontiersin.org 1 October 2017| Volume 8| Article 1966 fmicb-08-01966 October 5, 2017 Time: 15:18 # 2 Garbisu et al. Plasmid-Mediated Bioaugmentation for Contaminated Soils contaminated sites, with an annual estimated management cost Bioremediation has been successfully employed to remediate of 6 billion euros (Panagos et al., 2013). Different anthropogenic soils contaminated with organic contaminants, such as activities, such as combustion of fossil fuels, incineration, mining, aliphatic hydrocarbons, polycyclic aromatic hydrocarbons, agricultural practices, urbanization, waste disposal, etc. have polychlorinated biphenyls, organic solvents and so on (Maphosa contributed to the pressing problem of soil contamination (Besser et al., 2012). et al., 2009). Among other negative consequences, the presence The bioremediation of organic contaminants can be of contaminants in soil can cause a negative impact on the soil approached by three different strategies: bioattenuation, biota, resulting in an altered activity, biomass and/or diversity of biostimulation, and bioaugmentation (Figure 1A). soil biological communities (Burges et al., 2015). Bioattenuation relies on natural processes to maintain the growth and degrading activity of native microbial populations, so that contaminants are biodegraded without human intervention, REMEDIATION OF SOIL CONTAMINANTS apart from the monitoring of contaminant dispersal and degradation rates. Instead, the term biostimulation refers to the Traditionally, a variety of physicochemical methods adjustment of the environmental conditions (e.g., temperature, (e.g., excavation and disposal in landfills, soil washing, chemical moisture, aeration, pH, redox potential) and the application of oxidation, encapsulation, thermal treatments, incineration, nutrients (e.g., nitrogen, phosphorus) and electron acceptors to vitrification, solidification, etc.) have been used for soil contaminated soil, in order to enhance the growth of degrading remediation. However, these physicochemical strategies are microbial populations and, then, reduce the concentration of often expensive and, many times, reduce the concentration of soil contaminants. Finally, bioaugmentation has been defined soil contaminants at the expense of damaging the integrity of as the inoculation into contaminated soils of microorganisms the soil ecosystem (Epelde et al., 2009; Gómez-Sagasti et al., with the ability to degrade the target contaminants (Maier, 2000; 2016). Heinaru et al., 2005). This inoculation can be performed with The main goal of any soil remediation technology must be only one strain or, alternatively, with a consortium of microbial not only to reduce the concentration of soil contaminants but to strains with diverse metabolic capacities. The advantage of restore soil quality (Epelde et al., 2010; Barrutia et al., 2011; Pardo using a consortium of different strains is that toxic intermediate et al., 2014). A variety of soil physicochemical and biological products generated by one strain may be degraded by another properties (e.g., parameters that provide information on the strain (Heinaru et al., 2005). Apart from inoculating wild biomass, activity and diversity of soil microbial communities) strains with the required degradation capacities, laboratory- (Epelde et al., 2009; Muñoz-Leoz et al., 2013) are often used as constructed strains with upgraded catabolic abilities have also indicators of soil quality. It has also been proposed to assess the been considered for a more efficient bioaugmentation (Mrozik effectiveness of remediation methods in terms of the recovery of et al., 2011). soil ecosystem services and/or attributes of ecological relevance, Iwamoto and Nasu(2001) and El Fantroussi and Agathos such as organization, stability, redundancy, etc. (Garbisu et al., (2005) have proposed to apply bioaugmentation in those 2011; Epelde et al., 2014). cases where biostimulation and natural attenuation are As an alternative to physicochemical treatments, several proven ineffective. In this regard, in a diesel-contaminated biological methods of soil remediation, included within the soil, Bento et al.(2005) found bioaugmentation to be more terms bioremediation and phytoremediation, are currently effective for the degradation of the light fraction (C12–C23) of receiving much attention, mainly owing to their lower cost petroleum hydrocarbons than biostimulation. No significant and environmentally friendly character (Juwarkar et al., 2014). differences were detected between biostimulation and Bioremediation, or the use of microorganisms (bacteria, fungi) bioaugmentation in relation to the removal of the heavy to break down contaminants, takes advantage of the catabolic fraction (C23–C40). capacity of microorganisms to remove contaminants from soil. Bioaugmentation can be divided into two different However, bioremediation is effective only with a limited range approaches: (i) cell bioaugmentation, which relies on the of contaminants and contaminant concentrations. In addition, survival and growth of the inoculated strains to perform bioremediation techniques might take too long to achieve the the degradation of the target contaminants, and (ii) genetic desired reduction in the concentration of soil contaminants bioaugmentation, based on the spread of catabolic genes, located (Kumavath and Deverapalli, 2013). in mobile genetic elements (MGEs), into native microbial In relation to trace elements (a group of non-degradable populations. contaminants of much concern due to their well-known toxicity), However, despite decades of bioremediation research, the real microorganisms can only transform them from one oxidation drivers governing the degradation of organic contaminants are state or organic