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1 Xxvii Cycle Polluted Marine Ecosisistems UNIVERSITÀ DEGLI STUDI DI MILANO FACULTY OF AGRICULTURAL AND FOOD SCIENCE THE DEPARTMENT OF FOOD ENVIRONMENTAL AND NUTRITIONAL SCIENCES PHILOSOPHY DOCTORATE SCHOOL IN MOLECULAR SCIENCE AND AGRICULTURAL, FOOD AND ENVIRONMENTAL BIOTECHNOLOGY PHILOSOPHY DOCTORATE COURSE IN CHEMISTRY, BIOCHEMISTRY AND ECOLOGY OF PESTICIDES XXVII CYCLE PHILOSOPHY DOCTORATE THESIS POLLUTED MARINE ECOSISISTEMS: RESERVOIR OF MICROBIAL RESOURCES FOR HYDROCARBONS BIOREMEDIATION MARTA BARBATO NO. MATR. R09704 SUPERVISOR: PROFESSOR DANIELE GIUSEPPE DAFFONCHIO COORDINATOR: PROFESSOR DANIELE GIUSEPPE DAFFONCHIO ACADEMIC YEAR 2013/2014 1 2 CONTENTS Abstract 1 Riassunto 4 Chapter I RATIONALE AND AIM OF THE WORK 7 Chapter II THE MEDITERRANEAN SEA: AN UNEXPLOITED RESERVOIR 10 OF MICROBES FOR SITE-TAILORED HYDROCARBON BIOREMEDIATION STRATEGIES Chapter III BIOGEOGRAPHY OF PLANKTONIC BACTERIAL COMMUNITIES 33 ACROSS THE WHOLE MEDITERRANEAN SEA Chapter IV GENOTYPING OF Alcanivorax GENUS ISOLATES FROM THE 50 MEDITERRANEAN SEA HIGHLIGHT GEOGRAPHICAL DIVERGENCE Chapter V BEHAVIOR OF DIFFERENT HYDROCARBONOCLASTIC 67 BACTERIA STRAINS AT HIGH PRESSURE, SIMULATING OIL BIOREMEDIATION AT HIGH MARINE DEPTH Chapter VI BACTERIAL DIVERSITY AND BIOREMEDIATION POTENTIAL OF 79 THE HIGHLY CONTAMINATED MARINE SEDIMENTS AT EL-MAX DISTRICT (EGYPT, MEDITERRANEAN SEA) Chapter VII SEDIMENT DWELLING MICROBIOME RICHNESS AND THE 105 POTENTIAL FOR YDROCARBON REMEDIATION ARE DRIVEN BY POLLUTANTS’ TYPE AND CONCENTRATION: THE ANCONA HARBOR CASE-STUDY Chapter VIII ALLOCHTHONOUS BIOAUGMENTATION IN EX-SITU 127 TREATMENT OF CRUDE OIL POLLUTED SEDIMENTS IN THE PRESENCE OF AN EFFECTIVE DEGRADING INDIGENOUS MICROBIOME Chapter IX GENERAL CONCLUSION AND FUTURE PERSPECTIVES 140 Appendix 144 Acknowledgement 157 3 4 ABSTRACT Hydrocarbon (HC) pollution is a worldwide threat to marine natural ecosystems due to the increasing exploitation of underground marine petroleum deposits in several areas and to the high traffic of oil tankers and the presence of submarine pipes that are main transport routes for crude oil and refined products. HCs spread in the marine environment is mainly due to accidental oil spills or inadequate practices and their release affects marine ecosystems causing severe ecological and economical damages. The Mediterranean Sea is particularly endangered by hydrocarbon pollution because of its physical nature – it is an enclosed basin with a slow water exchange – and because it hosts about 20% of the global oil tanker traffic in its waters and tens of oil-related sites along its coastline. The conventional remediation strategies, comprising chemical and physical methods, are extremely expensive and invasive, therefore the development of cheaper and eco-friendly approaches is crucial to preserve human and ecosystem health. In this perspective, bioremediation (i.e. the use of living organisms to remove pollutants from a contaminated area) is a promising technology which, taking advantage of microbes’ metabolic potential to degrade a wide range of pollutants, can both reduce the costs and may represent a permanent solution. Nevertheless, there is still a scarce knowledge of the processes and the microorganisms involved in the clean-up of hydrocarbons from marine environments, hence some problems still exist concerning the in-field application of bioremediation. The aim of the present PhD thesis was to: i) investigate the overall prokaryotic diversity of pristine and oil polluted sites across the whole Mediterranean Sea; ii) depict the phylogenetic and functional diversity of hydrocarbonoclastic bacteria inhabiting pristine and polluted sites; iii) establish a large collection of bacteria showing degrading activities toward hydrocarbon compounds; iv) set up microcosm experiments to investigate the potential of bacterial bioaugmentation in bioremediation processes under laboratory scale conditions, v) test the degrading potential of selected bacterial strains and consortia under different pressure values, simulating different depths along the water column. The diversity of planktonic bacterial communities in the Mediterranean Sea was firstly evaluated on open seawater samples collected at different depths in a transect covering the main oil tanker route across the whole basin, from the Levantine Sea to the Gibraltar strait. Automated Ribosomal Intergenic Spacer Analysis (ARISA) showed that the microbiome inhabiting deep and surface water samples were sharply separated. Furthermore, the composition of the bacterial communities described in the surface layers of the water columns at different sampling stations has been significantly correlated, beside to their geographical position and depth, to the temperature and salinity values recorded for each sample. Denaturing Gradient Gel Electrophoresis (DGGE) and ARISA fingerprinting were also applied to depict the bacterial composition of highly polluted sediments collected at the Ancona harbor (Italy) and El-Max district (Egypt), showing the significant influence of the different pollutants’ concentration (i.e. hydrocarbons, heavy metals) in the selection of peculiar bacterial assemblages . This molecular approach led to the identification of bacterial species potentially useful for site-tailored bioremediation purposes. A large collection of hydrocarbon degrading bacterial strains was hence established from enrichments using contaminated sediments as inoculum and diesel, crude oil and naphthalene as unique carbon sources. The cultivation approaches adopted to enrich and isolate hydrocarbonoclastic bacteria from chronically polluted area, like the Ancona harbor, permitted to evaluate the influence of different hydrocarbon pollutants used as single carbon source in the selection of specific marine bacteria populations. The results obtained taking advantage of DGGE fingerprinting and 16S rRNA pyrosequencing applied on the enrichments showed that, under laboratory conditions, the supply of different hydrocarbon compounds led to the selection of different, and specialized, bacterial communities. A total of 248 bacterial strains have been isolated from open sea surface water collected along oil tanker routes and the chronically polluted sediments, and have been identified by 16S rRNA gene sequencing. Alcanivorax and Marinobacter, two ubiquitous marine hydrocarbonoclastic genera, were the most abundant within the established collection, representing respectively 67% and 23% of the isolates. Due to the great importance of the Alcanivorax genus for hydrocarbon remediation of marine polluted sites, all the isolates belonging to this genus were investigated at a finer level in terms of phylogenetic and functional diversity. This sub-collection, comprising 179 isolates belonging to the 4 species A. borkumensis, A. jadensis, A. venustensis and A. dieselolei, were genotyped using two different fingerprinting techniques: Internal Transcribed Spacer (ITS)-PCR and BOX-PCR. The combination of the applied techniques allowed the identification of 85 genotypes, distributed among the different sites investigated, showing clear evidence of geographic divergence. The functional diversity of these strains was furthermore investigated through the PCR amplification of the alkB gene, encoding for an alkane monooxigenase involved in the first step of hydrocarbons degradation, and subsequent Restriction Fragment Length Polymorphism (RFLP) analysis of the amplicons, allowing the identification of 16 different polymorphisms. The results demostrated the existence of a high degree of geographical divergence within the Alcanivorax genus, suggesting a potentially high metabolic diversity that could be exploited for site-tailored bioremediation interventions. 1 Recently, the Deepwater Horizon break in the Gulf of Mexico (2010) and the subsequent huge oil spill occurred at a depth of 1500 meters, highlighted the need to get more insight on bioremediation processes occurring at high depth. This accident represents a milestone and shed a light on the importance to investigate the effect of pressure, an environmental parameter that might hamper the activity of oil- degrading strains, on growth and degradation capabilities. The capability of selected hydrocarbonoclastic strains, belonging to the species A. jadensis, A. dieselolei and M. hydrocarbonoclasticus, to adapt and degrade a model alkane molecule (dodecane) at high pressure was therefore tested. The growth of the strains at increasing hydrostatic pressure and their physiologic activities were evaluated, comparing the results with the type strain A. borkumensis SK2. Overall, the results showed a detrimental effect of pressure for all the strains in terms of growth rates, O2 consumption and CO2 production. The potential adaptation of A. borkumensis and A.dieselolei was evaluated also with less recalcitrant carbon source than alkanes (pyruvate), without showing substantial differences, except for the higher consumption of pyruvate by A. borkumensis SK2. This investigation pinpointed that the tested bacteria can survive at high hydrostatic pressures, even though both their growth and degradation capability were mostly inhibited with the increase in hydrostatic pressure. Moreover, aiming to create a baseline for future transcriptomic analyses, the complete genome of this 4 strains was sequenced and annotated: all the strains owned multiple copies of the genes involved in the degradation of hydrocarbons (alkane monoossigenase, alk and cytochrome p450, cyp450), apparently belonging to different families, highlighting the great functional
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