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Bacteria, Fungi and Microalgae for the Bioremediation of Marine Sediments Contaminated by Petroleum Hydrocarbons in the Omics Era

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Bacteria, Fungi and Microalgae for the Bioremediation of Marine Sediments Contaminated by Petroleum Hydrocarbons in the Omics Era microorganisms Review Bacteria, Fungi and Microalgae for the Bioremediation of Marine Sediments Contaminated by Petroleum Hydrocarbons in the Omics Era Filippo Dell’ Anno 1,*, Eugenio Rastelli 2, Clementina Sansone 1 , Christophe Brunet 1, Adrianna Ianora 1 and Antonio Dell’ Anno 3,* 1 Department of Marine Biotechnology, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121 Naples, Italy; [email protected] (C.S.); [email protected] (C.B.); [email protected] (A.I.) 2 Department of Marine Biotechnology, Stazione Zoologica “Anton Dohrn”, Fano Marine Centre, Viale Adriatico 1-N, 61032 Fano, Italy; [email protected] 3 Department of Life and Environmental Sciences, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy * Correspondence: fi[email protected] (F.D.A.); [email protected] (A.D.A.) Abstract: Petroleum hydrocarbons (PHCs) are one of the most widespread and heterogeneous organic contaminants affecting marine ecosystems. The contamination of marine sediments or coastal areas by PHCs represents a major threat for the ecosystem and human health, calling for urgent, effective, and sustainable remediation solutions. Aside from some physical and chemical treatments that have been established over the years for marine sediment reclamation, bioremediation approaches based on the use of microorganisms are gaining increasing attention for their eco-compatibility, and lower costs. In this work, we review current knowledge concerning the bioremediation of PHCs in Citation: Dell’ Anno, F.; Rastelli, E.; Sansone, C.; Brunet, C.; Ianora, A.; marine systems, presenting a synthesis of the most effective microbial taxa (i.e., bacteria, fungi, and Dell’ Anno, A. Bacteria, Fungi and microalgae) identified so far for hydrocarbon removal. We also discuss the challenges offered by Microalgae for the Bioremediation of innovative molecular approaches for the design of effective reclamation strategies based on these Marine Sediments Contaminated by three microbial components of marine sediments contaminated by hydrocarbons. Petroleum Hydrocarbons in the Omics Era. Microorganisms 2021, 9, Keywords: marine sediments; petroleum hydrocarbons; hydrocarbonoclastic bacteria; fungi; mi- 1695. https://doi.org/10.3390/ croalgae; biostimulation; bioaugmentation; genome mining microorganisms9081695 Academic Editor: Carlos A. Jerez 1. Introduction Received: 12 July 2021 Different chemical contaminants, such as heavy metals and metalloids, aliphatic Accepted: 3 August 2021 Published: 10 August 2021 and polycyclic aromatic hydrocarbons, and halogenated compounds, are introduced in the marine environment by multiple sources (e.g., improper industrial discharges, waste Publisher’s Note: MDPI stays neutral disposal practices, combustion, continental runoff [1,2]). Such pollutants represent a serious with regard to jurisdictional claims in risk for marine biodiversity as well as the provision of ecosystem goods and services for published maps and institutional affil- human wellbeing [3]. Negative impacts are even more accentuated in coastal ecosystems, iations. characterized by high anthropic pressure and reduced hydrodynamic regime, which may lead to a high accumulation of chemical contaminants in the sediment [4]. Petroleum hydrocarbons (PHCs) contaminating aquatic environments are mainly composed of three classes of compounds: alkanes, olefins, and aromatics [5]. The PHCs, due to poor solubility in water, are adsorbed by particulate matter showing Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. a long-term persistence on the bottom of sediments with a significant negative impact on This article is an open access article benthic aquatic communities [6,7]. distributed under the terms and Different physicochemical techniques have been developed to reduce pollutant concen- conditions of the Creative Commons trations from water (e.g., based on chemical precipitation, ion-exchange, reverse osmosis, Attribution (CC BY) license (https:// electro-dialysis, and ultrafiltration) [8] or for ex-situ treatments of contaminated sediments creativecommons.org/licenses/by/ (e.g., based on chemical, electrochemical, and thermal strategies) [9,10]. However, there 4.0/). is an urgent need to find sustainable and eco-compatible solutions for the remediation of Microorganisms 2021, 9, 1695. https://doi.org/10.3390/microorganisms9081695 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 23 Microorganisms 2021, 9, 1695 2 of 22 sediments (e.g., based on chemical, electrochemical, and thermal strategies) [9,10]. How- ever, there is an urgent need to find sustainable and eco-compatible solutions for the re- mediation of contaminated sediments in situ. Accordingly, international policies (WFD contaminated2000/60 EU [11] sediments) are increasingly in situ. seeking Accordingly, management international alternatives policies able (WFD to reduce 2000/60 sedi- EU [11]) arement increasingly handling interventions, seeking management especially by alternatives promoting eco able-compatible to reduce technologies sediment handling for the inter- ventions,decontamination especially of polluted by promoting matrices. eco-compatible Bioremediation, technologies an environmental for the-friendly decontamination and of pollutedlow-cost matrices.strategy [12] Bioremediation,, relies on the ability an environmental-friendly of microorganisms (including and low-cost prokaryotes, strategy [12], reliesfungi onand the microalgae) ability of to microorganisms reduce contaminant (including concentrations prokaryotes, and/or their fungi toxicity and microalgae)(Figure to reduce1) [13]. contaminant concentrations and/or their toxicity (Figure1)[13]. FigureFigure 1.1. General scheme scheme of ofbioremediation bioremediation strategies strategies involving involving different different microbi microbialal taxa. taxa. CommonCommon microbial microbial-based-based bioremediation bioremediation strategies strategies include include the addition the addition of specific of specific compoundscompounds to to stimulate stimulate autochthonous autochthonous microbial microbial assemblages assemblages (biostimulation) (biostimulation) and/or and/or thethe additionaddition of of specific specific microbial microbial taxa, taxa, which which display display useful useful biodegradation/detox biodegradation/detoxificationification capacitycapacity (bioaugmentation [14 [14–18]–18). ]). Microbial taxa potentially beneficial for the bioremediation of contaminated sedi- Microbial taxa potentially beneficial for the bioremediation of contaminated sediments ments can be originally from the same area, or can be isolated from other contaminated can be originally from the same area, or can be isolated from other contaminated areas [19,20]. areas [19,20]. The use of autochthonous microorganisms is expected to be more effective Theand useecologically of autochthonous friendly, since microorganisms these are likely is expectedbetter adapted to be to more the specific effective local and envi- ecologically friendly,ronmental since conditions these are than likely allochthonous better adapted microbes, to the which specific may require local environmental the manipulation conditions thanof the allochthonous natural environment microbes, to maxi whichmize may their require performance the manipulation (e.g., changing of the oxygen natural and/or environment tonutrient maximize concentration, their performance pH [21]). (e.g., changing oxygen and/or nutrient concentration, pH [21]). AmongAmong bacteria bacteria involved involved in bioremediation in bioremediation processes, processes, most belong most belong to the genera to the Al- genera Al- caligens,caligens, Achromobacter, Acinetobacter, Acinetobacter, Alteromonas, Alteromonas, Arthrobacter, Arthrobacter, Burkholderia, Burkholderia, Bacil- Bacillus, Enterobacter,lus, Enterobacter, Flavobacterium, Flavobacterium, Pseudomonas Pseudomonas [22 [22,23],23]. Moreover,. Moreover, genera genera such such as as Alcanivorax, Al- Marinobacter,canivorax, Marinobacter, Thallassolituus, Thallassolituus, Cycloclasticus, Cycloclasticus, and Oleispira and Oleispira include include hydrocarbonoclastic hydrocar- bacteriabonoclastic (OHCB) bacteria and (OHCB) are known and are for known their for specific their specific ability ability to degrade to degrade hydrocarbons hydrocar- [24]. bons [24]. Besides bacteria, fungi have been described for their ability to produce particular Besides bacteria, fungi have been described for their ability to produce particular en- enzymes (e.g., catalases, peroxidases, laccases) able to degrade organic contaminants zymes (e.g., catalases, peroxidases, laccases) able to degrade organic contaminants and/or and/orto immobilize to immobilize inorganic contaminants inorganic contaminants [25,26]. Fungi [belonging25,26]. Fungi to the belonginggenera Aspergillus to the, genera Aspergillus, Curvularia, Drechslera, Fusarium, Lasiodiplodia, Mucor, Penicillium, Rhizopus, Trichoderma were reported as able to degrade aromatic hydrocarbons [27–29]. Microalgae, mainly green algae, belonging to the genera Selenastrum, Scenedemus, or Chlorella, have been demonstrated to be effective in the degradation of polycyclic aro- matic hydrocarbons, such as naphthalene, phenanthrene, and pyrene [30–33] and in the immobilization of metals. The mechanisms enabling microalgae to remove toxic com- pounds, thus reducing their bioavailability and toxicity, mainly rely on the production of exopolysaccharides, which
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