Biodegradation in the context of microbial consortia
Several organic compounds are recalcitrant to physical-chemical degradation, whereas, even in environments where biological degradation is possible, single organisms may lack the entirety of the necessary metabolic toolbox for achieving accelerated biodegradation. Microbial interactions in natural environments can extend and enhance the metabolic capacity and versatility of their constituting individual microbes as required by such compounds.
Enriched microbial communities can result in highly capable microbial consortia of degrading one or more recalcitrant organic pollutants simultaneously. Such catabolic activities are ususally coordinated via multimodular signaling cascades involving several members of the consortia. Signaling modes encompass: contact-independent communication based on quorum sensing molecules, electron exchange via electron carriers, cross-feeding, vitamin or amino-acid auxotrophy; and contact-dependent cell-cell interactions (e.g. DNA/protein exchange through the secretion systems, or even the presence of nanowires). This way biological networks are formed, and a variety of co-existence motifs (commensalistic, amensalistic, neutral, predatory/parasitic, cooperative) can be observed throughout the several stages of the degradation of the target recalcitrant compound(s).
The accelerated metabolic rates of the target compounds, the consortial population dynamics, and the linked communication modes, comprise essential elements for the potential use of tailor made consortia in bioaugmentation depuration strategies.
Our model system
Thiabendazole (TBZ), commonly used in fruit-packaging to control postharvest fungal diseases is a recalcitrant compound with a half-life of more than 2 years (DT50=833-1100 days) in soils (US EPA, 2002). It is a broad spectrum fungicide and although its mode of action is unclear, it is known to act as chelating agent found to affect fumarate reductase in nematodes (Prichard, 1970), while interference with the respiration and in particular the a terminal electron transport inhibition as also with the function of β-tubulin was observed in fungi (Allen and Gottlieb, 1970; Cabañas et al., 2009). Despite the standard tests carried out on eukaryotic marker organisms (US EPA, 2002), the effects of the parent compound and its metabolites on the microorganisms responsible for major biogeochemical cycles are largely unknown.
Recently, positive feedback of TBZ application was observed on soil nitrification activity, not affecting, however, the number of ammonia oxidizers, during a study released by our lab members in Papadopoulou et al (Papadopoulou et al., 2016). On the other hand, being a broad-spectrum fungicide, TBZ mediated growth suppression has been observed on beneficial fungi like e.g. the case of organisms designated for use biocontrol of plant pathogens (e.g. affected taxa include the Verticillium biguttatum, biocontrol agent of Rhizoctonia) (van den Boogert and Luttikholt, 2004), or arbuscular mycorrhizal fungi (AMF) at TBZ treated potato-seeds (Jin et al., 2013).
Regardless the surrogate biomarker, TBZ application was able to alter the individual-to-community microbial traits in the tested environments in several studies, particularly when applied at high doses. In the absence of suitable and affordable treatment systems, TBZ is frequently discharged via land spreading, leading to its accumulation in agricultural soils at high levels reaching concentrations of even 12 mg g-1 soil (Papadopoulou et al., 2015; Papadopoulou et al., 2016). Thus, the development of new and economically viable approaches for enhancing the on-site degradation of pesticides like TBZ, is mandatory.
Repeated microbial enrichment from soil derived from a fruit-packaging industry waste-disposal site resulted in the cultures of a microbial consortium able to degrade TBZ in just a few days as described in the study performed in our lab by Perruchon et al (Perruchon et al., 2017a). The consortium was screened by means of denaturant gradient gel electrophoresis (DGGE) and stable isotope probing (SIP) DGGE of the 16S rRNA marker gene partial amplicons, and cloning. Results showed that it was composed by Shinella, Oligotropha, Sphingomonas, Methilibium, Methylobacillus, Hydrogenophaga, Pseudomonas and Hydrocarboniphaga strains. In this detailed study, antibiotic selectivity and SIP-DGGE suggested the dominant roles of the Sphingomonas and the Hydrogenophaga strains to the TBZ degradation, while thiazole-4-carboxamidine was proposed as a key metabolite in the TBZ degradation.
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