Research articleRemoval of Quebracho and Tara tannins in fungal bioreactors: Performance and biofilm stability analysis
Graphical abstract
Introduction
Tannins are abundantly applied in leather tanning industry due to their prerogative of precipitating proteins (Lorenz et al., 2014). In fact, tannins blind to the collagen proteins of the animal skin making leather more durable and not putrescible. Tannins are water-soluble polyphenolic compounds produced by plants (Barbehenn and Peter Constabel, 2011) and could be subdivided into hydrolysable (gallotannins and ellagitannins), condensed (or proanthocyanidins) and complex tannins (Khanbabaee and Ree, 2001). Tara tannin (TT) is obtained from the fruit pods of Cæsalpinia spp., which principal components are hydrolysable tannins based on a galloylated quinic acid structure (Sciences et al., 2007). Quebracho tannin (QT) is obtained from the wood of Schinopsis spp. and is composed mainly of condensed tannins that are more difficult to be biodegraded than those found in TT given that hydrolysable tannins are easier to be biodegraded (He et al., 2008). Conventional activated sludge systems (Li et al., 2009) and anaerobic digestion (Mannucci et al., 2010) are not effective to treat tannins due to their low biodegradability and high soluble chemical oxygen demand (sCOD) (Lofrano et al., 2013). In fact, high concentration of tannins can inhibit the biological treatment (Munz et al., 2009). Then, tannins are usually removed by means of chemical processes in tannery wastewater treatment plants (WWTPs).
Although the leather tanning industry is known to be of prime economic importance in many countries, the concern about the environmental impacts related to the production of leather and the release of various recalcitrant pollutants in tannery wastewaters (Lofrano et al., 2013; Romer et al., 2011) has been increasing in the last decades. Current biological wastewater treatments are engineered biological ecosystems based on bacteria, which are ineffective in the removal of several recalcitrant compounds such as tannins (Mannucci et al., 2010). Fungi play a role in the biodegradation of phenols, chlorinated phenolic compounds, chlorinated alkanes and alkenes, polycyclic aromatic hydrocarbons, petroleum hydrocarbons and other emerging contaminants (Harms et al., 2011). Although fungi represent a promising biological resource in environmental biotechnology, they have rarely been applied in wastewater treatment due to a lack of knowledge regarding the optimal process conditions and due to their lack of stability under non-sterile conditions (Espinosa-Ortiz et al., 2016). Most research in wastewater treatment with fungi has been focused on the degradation of pharmaceuticals, dyes and pesticides at lab-scale, with important limitations and, above all, mostly under sterile conditions (Svobodová and Novotný, 2017). In fact, the main operational concerns are related to bacterial contamination and to the robustness of the bioprocess in the long-run since fungi are easily outcompeted by bacteria. Nowadays, operation of a fungal-based bioreactor able to maintain stable fungal growth and performance, under sterile and non-sterile conditions, is still challenging. Furthermore, the fungal degradation of most recalcitrant compounds frequently requires the supply of an external carbon source (co-substrate), since recalcitrant compounds might not be suitable substrates for fungal growth (Palli et al., 2016). Nevertheless, among recalcitrant compounds present in tannery wastewaters, tannins represent a potential carbon source for fungi, despite their antimicrobial properties (Mingshu et al., 2006). Alternative biological treatment processes able to effectively remove this fraction could lead to environmental and economical advantages (Giaccherini et al., 2017). Moreover, Aspergillus spp. and Penicillium spp. have been isolated in tannery wastewaters and reported as microorganisms capable to biodegrade tannins (Murugan et al., 2007). In particular, Aspergillus (section Nigri) can grow on tannic acid (TA) as carbon source and was found in tannery wastewaters with high QT concentration (León-Galván et al., 2010). Based on this findings, it can be hypothesised that fungi would be able to grow in the recalcitrant fraction of wastewater containing a high concentration of tannins, such as tannery wastewater. Most of the research reported in the literature about the biodegradation of natural tannins and polyphenolic compounds by fungi has been performed in petri dishes or flasks using tea by-products (Ni et al., 2015), tannin extracts (Belmares et al., 2009) or on TA (Van Diepeningen et al., 2004). To the authors' knowledge, no previous experiments have been reported with continuously fed bioreactors (under sterile or non-sterile conditions) for the removal of QT, TT or other natural tannins with fungi.
The aims of the present work were i) to demonstrate the proper performance ii) to evaluate the stability and iii) to assess the bacterial and fungal diversity of a novel fungal bioreactor configuration operated under non-sterile conditions to reach an effective removal of Tara and Quebracho tannins. TT was selected as a representative of hydrolysable tannins and QT as a representative of condensed tannins, among the natural tannins applied as tanning agents. The evolution of the system was evaluated by means of combined physical-chemical analyses and molecular techniques for bacteria and fungi. Almost no works in literature have analysed both communities and their relationship during the treatment of tannins in bioreactors.
Section snippets
Fungal strain, immobilisation on supports and reagents
Based on previous tests (Tigini et al., 2015) and literature research, Aspergillus tubingensis MUT 990, a black Aspergillus belonging to the section Nigri, was chosen as the inoculum for the present study. This fungal strain was originally isolated from commercial TT powder and is preserved at Mycotheca Universitatis Taurinensis (MUT) on malt extract agar (MEA) (agar 20 g, glucose 2 g, malt extract 2 g, peptone 0.2 g, water up to litre) at 4 °C. The selected fungal strain was inoculated on 20
Performance of Quebracho tannin degrading reactor
Despite some oscillations occurred in the first 56 days, the sCOD-RE was ranging from 4% to 34% which was in average (17% ± 7%) higher than that determined from respirometric tests carried out with an activated sludge sample collected from a tannery WWTP (sCOD-RE of 8%) as shown in Fig. 2. This difference was related to the fungal biomass inoculated, which was more effective in QT removal than the autochthonous species of the activated sludge from the tannery WWTP. It may also depend on the
Conclusions
The effects of two different types of tannins, condensed and hydrolysable, on the fungal biomass were investigated and separately tested in two reactors. Fungal and bacterial consortia developed in the long-term operation of bioreactors fed with QT and TT after initial inoculation with Aspergillus tubingensis. Reactor fed with QT outlasted the colonisation of bacteria and allowed a stable fungal biofilm able to remove QT with RE up to 53%. Reactor fed with TT suffered the detachment of the
Acknowledgments
The authors thank the Miur (Fir project RBFR13V3CH), the UE (Marie Curie Irses Carbala project 295176) and the Tuscany region (Lightan POR FESR 2014-2020). Moreover, the authors thank Andrea Nardo for the support given with respirometric tests; Clara Reino for the support given with DNA extraction; Chimont International Spa for providing the tannins and the Mycoteca Universitatis Taurinensis (MUT) for providing the fungal strain.
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