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“Marine Biotechnologies for the Decontamination and Restoration of Degraded Marine Habitats”

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“Marine Biotechnologies for the Decontamination and Restoration of Degraded Marine Habitats” “Marine biotechnologies for the decontamination and restoration of degraded marine habitats” PhD Candidate: Filippo Dell’ Anno (F7057844) Thesis submitted for the degree of Doctor of Philosophy, XVIII Cycle November 2019 The Open University, Milton Keynes (UK), School of Life, Health and Chemical Sciences Stazione Zoologica Anton Dohrn Naples (Italy), Department of Marine Biotechnology 1 Supervision Pannel: Director of Studies: Dr. Adrianna Ianora (Stazione Zoologica Anton Dohrn, IT) Internal Supervisor: Dr. Clementina Sansone (Stazione Zoologica Anton Dohrn, IT) External Supervisor: Prof. Antonio Dell’ Anno (Università Politecnica delle Marche, IT) Advisor: Prof. Alan Dobson (University College Cork, Ireland) Examiners: External Examiner: Prof. Peter Golyshin (Bangor University, UK) Internal Examiner: Dr. Paolo Sordino (Stazione Zoologica Anton Dohrn, IT) Chair: Dr. Alessandra Gallo (Stazione Zoologica Anton Dohrn, IT) 2 Abstract This research presents the results obtained using a bioremediation approach aiming to enhance natural remediation of the Bagnoli-Coroglio area, a post industrial site in the Gulf of Naples, Italy, characterized by the presence of several pollutants released in almost a century by the ILVA steel plant. In particular, the thesis evaluates the benthic microbial taxonomic composition of this area after ten decades of pollution. Results indicate the prevalence of the Phyla Proteobacteria, (36.7%), Planctomycetes (20.5%) and Bacteroidetes (9.6%) and the presence of a core microbiome suggesting that pollutants and other abiotic factors may have contributed to shape benthic prokaryotic communities. The thesis also evaluates the biotechnological potential of single isolates bacteria (Halomonas sp., Alcanivorax sp., Epibacterium sp., Pseudoalteromonas sp., and Virgibacillus sp.) and mixtures of these species isolated from polluted sediments collected from Bagnoli-Coroglio area and the Sarno river mouth, another polluted site in the Gulf of Naples. Laboratory tests highlighted the ability of mixed cultures and single taxa to degrade PAHs (Polyclic Aromatic Hydrocarbons) and precipitate heavy metals from culture media. Results of Sequential Selective Extraction (SSE) analysis emphasized the ability of mixed cultures to reduce the mobility of As, Cd and Zn by changing their partitioning in the geochemical fractions. Full genome sequencing of isolated strains has allowed for the genetic and molecular characterization of mechanisms underlying processes of degradation and detoxification of xenobiotics. In particular, many genes involved in hydrocarbon degradation pathways and in heavy metal detoxification systems have been identified. My results suggest a potential biotechnological 3 application of these strains in waste-water treatment as well as decontamination of polluted sediments. Acknowledgements I would like to thank my supervisory team: Dr. Adrianna Ianora, Prof. Antonio Dell' Anno and Dr. Clementina Sansone. Their help was precious and fundamental to complete my thesis. A warm thanks to my Advisor, Prof Alan Dobson, who during these years has given me valuable advice to guide my research. I am also very grateful to Prof. Marla Trinidade and Dr. Lonnie van Zyl from IMBM (University of Western Cape, SA) who allowed me to deeply investigate the genomic features belonging to the isolated bacteria, during a three month secondment funded by the EU Ocean Medicines (H2020, MSCA-RISE) project. Finally, I would like to thank my family who, unconditionally, supported me during these years, and Francesca that makes my life every day brighter. 4 Table of contents Table of contents Chapter 1: General Introduction……………………………………………………………………………….1 1.1) Bioremediation: state of art…………………………………………………………………………………..1 1.2) PAHs bacterial remediation………………………………………………………………....................10 1.3) Heavy metals bacterial remediation…………………………………………………....................18 1.4) Towards an Omicss bioremediation approach ………………………………….....................29 1.5) Aims of the thesis……………………………………………………………………………..................... 33 Chapter 2: Effects of multiple pollution stressors on microbial diversity: The case study of the Bagnoli-Coroglio area (Gulf of Naples, South Tyrrenhian Sea).…….………………………………………………………………………………………………………………..35 1) Introduction…………………………………………………………………………………………………………..36 2) Material and Methods……………………………………………………………………………………………38 2.1) Study area…………………………………………………………………………………………………………..38 2.2) Prokaryotic Abundance and Biomass………………………………………………......................40 2.3) Illumina sequencing and bioinformatic procedures for sediment microbiome analyses………………………………………………………………………………........................................41 2.4) Statistical analyses………………………………………………………………………………………………42 3) Results and discussion………………………………………………………………………………………..43 3.1) Chemical characterization……………………………………………………………………………………43 3.2) Prokaryotic Abundance……………………………………………………………………………………….46 3.3) Alpha diversity…………………………………………………………………………………………………….49 3.4) Taxonomic composition……………………………………………………………………………………….52 4) Conclusion……………………………………………………………………………………………….…………64 Chapter 3: Biotechnological potential of bacteria isolated from two highly anthropic- impacted coastal areas from the Gulf of Naples.…………………………………………………….65 5 Abstract………………………………………………………………………………………………………………….65 1)Introduction……………………………………………………………………………………………………………67 2)Material and Methods…………………………………………………………………………………………….69 2.1) Sediment sampling……………………………………………………………………………………………..69 2.2) Bacteria isolation from sediments from both sites………………………………………………71 2.3) Bacteria characterization and identification………………………………………………………..72 2.4) Analysis of sequenced data………………………………………………………………………………….72 2.5) Bacteria growth versus metals and PAHs concentrations…………………………………….72 2.6) Evaluation of Polycyclic Aromatic Hydrocarbons (PAHs) degradation and removal rate of heavy metals in liquid solution………………………………………………………………………..73 2.7) Evaluation of Polycyclic Aromatic Hydrocarbons (PAHs) degradation and removal rate of heavy metals during coupled water-sediment experiments……………………………………………………………………………………………………………….75 3)Results and Discussion…………………………………………………………………………………………76 3.1) Bioremediation of Bacteria Isolated from the Sarno River Site……………………………..76 3.1.1) Identification of bacterial isolates and bacterial growth in the presence of contaminants ……….……………………………………………………………………………………………………76 3.1.2) Evaluation of PAHs degradation and heavy metal precipitation of bacterial cultures (as single isolate and in mixtures)……………….………………………………………………..89 3.1.3) Effects of bacterial cultures addition (as isolates and as mixtures) on hydrocarbon degradation and heavy metal partitioning in contaminated sediments from Bagnoli-Coroglio………………………............................................................................95 3.2) Bioremediation of Bacteria Isolated from the Bagnoli-Coroglio Site…………………….99 3.2.1) Identification of bacterial isolates and bacterial growth in the presence of contaminants…………………….…………………………………….....................................................99 3.2.2) Evaluation of PAHs degradation and heavy metal precipitation capacity of bacterial cultures (as isolates and and in mixtures).…………………………………………………..115 3.2.3) Effects of bacterial cultures addition (as isolates and as mixtures) on hydrocarbon degradation and heavy metal partitioning in contaminated sediments from Bagnoli- Coroglio …………………………………………………………………………..……………………………………..121 4)Conclusion…………………………………………………………………………………………………………127 6 Chapter 4: Genomic characterization and functional analysis of bacterial isolates..128 Abstract……………………………………………………………………………………………………………….128 1) Introduction……………………………………………………………………………………………………..129 2) Materials and Method……………………………………………………………………………………...131 2.1) Bacterial culturing……………………………………………………………………………………………..131 2.2) Genomic DNA preparation and Genome sequencing………………………………………….131 2.3) Annotation and comparative genomics……………………………………………………………..132 3) Results and discussion…………………………………………………………………………………….…134 3. 1) General description of the Genomes…………………………………………………………………140 3.1.1) Halomonas sp. SZN1.………………………………………………………………………………………140 3.1.2) Alcanivorax sp. SZN2.………………………………………………………..…………………………...144 3.1.3) Pseudoalteromonas sp. SZN3………………………………………………………………………….148 3.1.4) Epibacterium sp. SZN4.…………………………………………………………………………………...151 3.1.5) Oceanicaulis sp. SZN5...…………………………………………………………………………………..155 3.1.6) Alkaliphilus sp. SZN6.………………………………………………………………………………………158 3.2) Genetic basis of PAHs degradation…………………………………………………………………….161 3.2.1) Ring Hydroxylating dioxygenase………………………………………………………………….….166 3.2.2) Cytochrome P450………………………………………………………………………………………..….173 3.2.3) Catechol pathway…………………………………………………………………………………………..179 3.2.4) Protocatechuate pathway……………………………………………………………………………...182 3.2.5) Homogentisate pathway…………………………………………………………………………………187 3.2.6) Homoprocatechuate pathway………………………………………………………………………..192 3.2.7) Phenilacetic pathway………………………………………………………………………………………197 3.3) Genetic bases for Metal detoxification………………………………………………………………201 4) Conclusion………………………………………………………………………………………………………..211 Chapter 5: General conclusions….………………………………………………………………………….213 6) Bibliography……………………………………………………………………………………………………..221 7 List of Figures Figure 1.1. Map of the four sampling sites analysed in the current study: 1) Impianto Sollevamento Dazio, 2) Scarico Conca di Agnano; 3) Canale Bianchettaro; 4) Galleria scarico Impianto Coroglio…………………………………………………………………………………………..39
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