Abstract
The concurrence of structurally complex petroleum-associated contaminants at relatively high concentrations, with diverse climatic conditions and textural soil characteristics, hinders conventional bioremediation processes. Recalcitrant compounds such as high molecular weight polycyclic aromatic hydrocarbons (HMW-PAHs) and heavy alkanes commonly remain after standard soil bioremediation at concentrations above regulatory limits. The present study assessed the potential of native fungal bioaugmentation as a strategy to promote the bioremediation of an aged industrially polluted soil enriched with heavy hydrocarbon fractions. Microcosms assays were performed by means of biostimulation and bioaugmentation, by inoculating a defined consortium of six potentially hydrocarbonoclastic fungi belonging to the genera Penicillium, Ulocladium, Aspergillus, and Fusarium, which were isolated previously from the polluted soil. The biodegradation performance of fungal bioaugmentation was compared with soil biostimulation (water and nutrient addition) and with untreated soil as a control. Fungal bioaugmentation resulted in a higher biodegradation of total petroleum hydrocarbons (TPH) and of HMW-PAHs than with biostimulation. TPH (C14-C35) decreased by a 39.90 ± 1.99% in bioaugmented microcosms vs. a 24.17 ± 1.31% in biostimulated microcosms. As for the effect of fungal bioaugmentation on HMW-PAHs, the 5-ringed benzo(a)fluoranthene and benzo(a)pyrene were reduced by a 36% and 46%, respectively, while the 6-ringed benzoperylene decreased by a 28%, after 120 days of treatment. Biostimulated microcosm exhibited a significantly lower reduction of 5- and 6-ringed PAHs (8% and 5% respectively). Higher TPH and HMW-PAHs biodegradation levels in bioaugmented microcosms were also associated to a significant decrease in acute ecotoxicity (EC50) by Vibrio fischeri bioluminiscence inhibition assays. Molecular profiling and counting of viable hydrocarbon-degrading bacteria from soil microcosms revealed that fungal bioaugmentation promoted the growth of autochthonous active hydrocarbon-degrading bacteria. The implementation of such an approach to enhance hydrocarbon biodegradation should be considered as a novel bioremediation strategy for the treatment of the most recalcitrant and highly genotoxic hydrocarbons in aged industrially polluted soils.
Highlights
The bioremediation of soil polluted with petroleum hydrocarbon has many advantages compared to physicochemical techniques, but it presents challenges due to the heterogeneity and variable concentration of contaminants, as well as the diverse site environmental conditions (Atlas and Philip, 2005; Singh, 2006)
Elemental analysis yielded a molar ratio C(carbon):H(hydrogen):N(nitrogen):S(sulfur) of 13:3:0.2:0.6, which indicated that the C:N ratio was slightly above the recommended values (25:1:1 to 38:1:1), according to Atagana (2009) and Alexander (1999), for the fungal polycyclic aromatic hydrocarbons (PAHs) bioremediation under an optimum water and oxygen content
During fungal biaugmentation the aliphatic-degrading bacteria achieved the highest counts in the late stages (60–120 days), with values above 107 most probable number (MPN) × g−1 (2.5 magnitude order higher than those observed in the BS treatment). Such high bacterial counts were coincident with the maximum biodegradation of Total Petroleum Hydrocarbons (TPH) of late stages in B (Figure 1). These results demonstrate that the inoculation of the autochthonous fungi promoted the establishment of active hydrocarbon-degrading bacterial populations that biodegraded both aliphatic hydrocarbons and PAHs in aged-polluted soils
Summary
The bioremediation of soil polluted with petroleum hydrocarbon has many advantages compared to physicochemical techniques, but it presents challenges due to the heterogeneity and variable concentration of contaminants, as well as the diverse site environmental conditions (Atlas and Philip, 2005; Singh, 2006). Previous studies have shown the advantages of fungi over bacteria for the biodegradation of HMW-hydrocarbons in contaminated soils (Aranda et al, 2017; Prenafeta-Boldú et al, 2019): (i) secretion of several low substrate specificity enzymes (e.g., laccases, lignin peroxidases, and Mn peroxidases) (Harms et al, 2011); (ii) osmo- and xerotolerance of several fungal species that confers an ability to grow in rather extreme and fluctuating environments (Worrich et al, 2017; González-Abradelo et al, 2019; Peidro-Guzmán et al, 2020); and (iii) the capacity of filamentous fungi to form mycelial networks that are often hydrophobic and that might cover several hectares of soil, enhancing the access to hydrocarbon contaminants (Wick et al, 2007; Furuno et al, 2012; Bielèik et al, 2019). These abilities are of particular interest in case of the less water soluble
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