Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons

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 hyd...

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Main Authors: María Cecilia Medaura, Miriam Guivernau, X. Moreno-Ventas, Francesc X. Prenafeta-Boldú, Marc Viñas
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.626436/full
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spelling doaj-b8c6b0e00fa64b2b8ce99e76207cf4a52021-03-31T06:25:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-03-011210.3389/fmicb.2021.626436626436Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy HydrocarbonsMaría Cecilia Medaura0Miriam Guivernau1X. Moreno-Ventas2Francesc X. Prenafeta-Boldú3Marc Viñas4Faculty of Engineering, National University of Cuyo, Mendoza, ArgentinaGIRO Program, Institute of Agrifood Research and Technology (IRTA), Caldes de Montbui, Barcelona, SpainDepartment of Sciences and Techniques in Water and Environment, University of Cantabria, Santander, SpainGIRO Program, Institute of Agrifood Research and Technology (IRTA), Caldes de Montbui, Barcelona, SpainGIRO Program, Institute of Agrifood Research and Technology (IRTA), Caldes de Montbui, Barcelona, SpainThe 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.626436/fullaged-polluted soilhigh molecular weight polycyclic aromatic hydrocarbonsmycoremediationnative-fungal-bioaugmentationfungal-bacterial interactionsindigenous hydrocarbonoclastic fungi
collection DOAJ
language English
format Article
sources DOAJ
author María Cecilia Medaura
Miriam Guivernau
X. Moreno-Ventas
Francesc X. Prenafeta-Boldú
Marc Viñas
spellingShingle María Cecilia Medaura
Miriam Guivernau
X. Moreno-Ventas
Francesc X. Prenafeta-Boldú
Marc Viñas
Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons
Frontiers in Microbiology
aged-polluted soil
high molecular weight polycyclic aromatic hydrocarbons
mycoremediation
native-fungal-bioaugmentation
fungal-bacterial interactions
indigenous hydrocarbonoclastic fungi
author_facet María Cecilia Medaura
Miriam Guivernau
X. Moreno-Ventas
Francesc X. Prenafeta-Boldú
Marc Viñas
author_sort María Cecilia Medaura
title Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons
title_short Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons
title_full Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons
title_fullStr Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons
title_full_unstemmed Bioaugmentation of Native Fungi, an Efficient Strategy for the Bioremediation of an Aged Industrially Polluted Soil With Heavy Hydrocarbons
title_sort bioaugmentation of native fungi, an efficient strategy for the bioremediation of an aged industrially polluted soil with heavy hydrocarbons
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-03-01
description 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.
topic aged-polluted soil
high molecular weight polycyclic aromatic hydrocarbons
mycoremediation
native-fungal-bioaugmentation
fungal-bacterial interactions
indigenous hydrocarbonoclastic fungi
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.626436/full
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