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Allochthonous Bioaugmentation in Ex Situ Treatment of Crude Oil-Polluted Sediments in the Presence of an Effective Degrading Indigenous Microbiome

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Allochthonous Bioaugmentation in Ex Situ Treatment of Crude Oil-Polluted Sediments in the Presence of an Effective Degrading Indigenous Microbiome Allochthonous bioaugmentation in ex situ treatment of crude oil-polluted sediments in the presence of an effective degrading indigenous microbiome Item Type Article Authors Fodelianakis, Stylianos; Antoniou, E. A.; Mapelli, Francesca; Magagnini, Mirko; Nikolopoulou, Maria; Marasco, Ramona; Barbato, Marta; Tsiola, Areti; Tsikopoulou, I.; Giaccaglia, L.; Mahjoubi, Mouna; Jaouani, Atef; Amer, R.; Hussein, Emad I.; Al-Horani, Fuad A.; Benzha, Fatiha; Blaghen, Mohamed; Malkawi, Hanan Issa; Abdel-Fattah, Yasser Refaat; Cherif, Ameur; Daffonchio, Daniele; Kalogerakis, Nicolas E. Citation Fodelianakis, S., Antoniou, E., Mapelli, F., Magagnini, M., Nikolopoulou, M., Marasco, R., … Kalogerakis, N. (2015). Allochthonous bioaugmentation in ex situ treatment of crude oil-polluted sediments in the presence of an effective degrading indigenous microbiome. Journal of Hazardous Materials, 287, 78– 86. doi:10.1016/j.jhazmat.2015.01.038 Eprint version Post-print DOI 10.1016/j.jhazmat.2015.01.038 Publisher Elsevier BV Journal Journal of Hazardous Materials Download date 04/10/2021 09:38:01 Link to Item http://hdl.handle.net/10754/564116 1" Allochthonous bioaugmentation in ex situ treatment of crude oil-polluted 2" sediments in the presence of an effective degrading indigenous microbiome 3" 4" Fodelianakis S.1,2, Antoniou E.1, Mapelli F.3, Magagnini M.4, Nikolopoulou M.1 , Marasco 5" R.3,2, Barbato M.3, Tsiola A.5, Tsikopoulou I.5,6, Giaccaglia L.4, Mahjoubi M.7, Jaouani A.8, 6" Amer R.9, Hussein E.10, Al-Horani F.A.11, Benzha F.12, Blaghen M.12, Malkawi H.I.10, Abdel- 7" Fattah Y.9, Cherif A.7,8, Daffonchio D.3,2, Kalogerakis N.1* 8" 9" 1 School of Environmental Engineering, Technical University of Crete, Greece 10" 2 King Abdullah University of Science and Technology, Thuwal, Saudi Arabia 11" 3 Dept. of Food, Environment and Nutritional Sciences, University of Milan, Italy 12" 4 EcoTechSystems S.r.l., Italy 13" 5 Hellenic Center for Marine Research, Crete, Greece 14" 6 Department of Biology, University of Crete, Greece 15" 7 LR11-ES31 Biotechnology and Bio-Geo Resources Valorization, Higher Institute for Biotechnology, 16" Biotechpole SidiThabet, University of Manouba, 2020, Ariana, Tunisia 17" 8 Laboratory of Microorganisms and Active Biomolecules, Faculty of Sciences of Tunis, University of Tunis El 18" Manar, 2092, Tunis, Tunisia 19" 9 Genetic Engineering and Biotechnology Research Institute, City for Scientific Research and Technology 20" Applications (SRTA-City), Alexandria, Egypt 21" 10 Department of Biological Sciences, Yarmouk University, 211-63, Irbid-Jordan 22" 11 Faculty of Marine Sciences, The University of Jordan-Aqaba, 7110, Aqaba-Jordan 1" " 23" 12 Laboratory of Microbiolgy, Biotechnology and Environmrent, University Hassan II Casablanca, Faculty of 24" Sciences aîn-chock, B.P.5366, Morocco 25" *Address correspondence to: Nicolas Kalogerakis ([email protected] ), School of 26" Environmental Engineering, Technical University of Crete, Polytechneioupolis, Chania, 73100, Greece. Tel.: 27" +302821037794, Fax: +30-28210-37852 2" " 28" Abstract 29" Oil-polluted sediment bioremediation depends on both physicochemical and 30" biological parameters, but the effect of the latter cannot be evaluated without the optimization 31" of the former. We aimed in optimizing the physicochemical parameters related to 32" biodegradation by applying an ex-situ landfarming set-up combined with biostimulation to 33" oil-polluted sediment, in order to determine the added effect of bioaugmentation by four 34" allochthonous oil-degrading bacterial consortia in relation to the degradation efficiency of the 35" indigenous community. We monitored hydrocarbon degradation, sediment ecotoxicity and 36" hydrolytic activity, bacterial population sizes and bacterial community dynamics, 37" characterizing the dominant taxa through time and at each treatment. We observed no 38" significant differences in total degradation, but increased ecotoxicity between the different 39" treatments receiving both biostimulation and bioaugmentation and the biostimulated-only 40" control. Moreover, the added allochthonous bacteria quickly perished and were rarely 41" detected, their addition inducing minimal shifts in community structure although it altered the 42" distribution of the residual hydrocarbons in two treatments. Therefore, we concluded that 43" biodegradation was mostly performed by the autochthonous populations while 44" bioaugmentation, in contrast to biostimulation, did not enhance the remediation process. Our 45" results indicate that when environmental conditions are optimized, the indigenous 46" microbiome at a polluted site will likely outperform any allochthonous consortium. 47" 48" Keywords: bioremediation, biostimulation, bioaugmentation, autochthonous degraders, 49" allochthonous degraders, landfarming, petroleum 3" " 50" 1. Introduction 51" Marine sands and sediments that are exposed to crude oil contamination are of major 52" concern worldwide [1, 2]. Although both physicochemical and biological treatment methods 53" exist for the remediation of such polluted environments, the use of the latter is continuously 54" increasing due to their much lower costs and environmental friendly nature [3-5]. 55" The remediation of oil-polluted sediments through biological means (bioremediation) 56" involves the use of microorganisms that are able to degrade the pollutants. Currently, studies 57" focus on enhancing the degradation potential of the indigenous microorganisms by altering 58" the physicochemical parameters that could potentially stimulate the community's metabolic 59" capacity (biostimulation), increasing the number of microorganisms that are capable of 60" degrading the pollutants (bioaugmentation), or a combination of the two. Many studies have 61" examined the effectiveness of each approach with contrasting results, and an ongoing 62" scientific debate of how physicochemical (e.g. temperature, humidity, sediment oxygenation 63" and grain size or organic matter content) or biological (e.g. long term survival of the added 64" microorganisms, antagonism with the indigenous populations, origin of the added strains) 65" parameters determine the efficiency of each approach [3, 6-10]. 66" One of the major bottlenecks of any applied method that is based on degradation by 67" aerobic microorganisms in situ, is the often-poor oxygen availability within the sediments 68" that can severely limit degradation. The simplest method used to overcome oxygen limitation 69" is ex situ treatment by landfarming, a technique that involves spreading of contaminated soils 70" (including beach sand), petroleum sludges or sediments in a thin layer (typically less than 25- 71" 30 cm) and regular tilling, combined with the addition of nutrients and water to maintain 72" moisture (typically about 20%). This method has been widely used in soil remediation for 4" " 73" over a century due to its low cost, simplicity in use, compliance with governmental 74" regulations and potential application in a variety of environments [1]. 75" The aim of the present study was to evaluate the effectiveness of bioaugmentation 76" with allochthonous hydrocarbon-degrading bacterial consortia in the bioremediation of oil- 77" contaminated sediments treated ex situ by landfarming, in the presence of the indigenous 78" microbiome and when the relevant physicochemical parameters are optimized. We setup an 79" experimental design to investigate the real advantage of bioaugmentation during landfarming 80" practices through the evaluation of degradation performance between the different tested 81" consortia and between allochthonous and indigenous degrading populations. An integrated 82" approach was adopted, allowing the monitoring of the degradation of different crude oil 83" compounds, and the dynamics in terms of enzymatic activity, community structure and 84" population sizes of the bacterial communities in each treatment. 85" 5" " 86" 2. Experimental 87" 2.1 Sediment sampling and experimental setup 88" Polluted sediment (c.a. 30 L) was collected on January 14, 2013, from a coast 89" adjacent to an oil refinery (Elefsina bay, Greece, 38° 2'16.28"N, 23°30'45.85"E), where 90" hydrocarbon releases occur intermittently, and was transferred to the lab overnight, in a 50 L 91" plastic barrel. A detailed physicochemical characterization of the sediment is given in Table 92" S1. The initial sediment contamination was estimated at 5000 ppm of crude oil per gram of 93" sediment, using soxhlet extraction (Table S1). Upon arrival to the lab on the next day, 94" sediment was filtered through a 5 mm sieve in order to remove large particles that could 95" interfere with all downstream analyses, and was air-dried down to 20% humidity (w/w). 96" Sediment temperature was monitored constantly, remaining within the 10-20 °C range. 97" When sediment reached the desired humidity (20%), total heterotrophic bacterial 98" colony forming units (CFUs) per gram of sediment were determined (see below) and 99" sediment was placed within nine glass microcosms (1.4 L, 19 cm x 18.5 cm x 4 cm, open top) 100" with 1.5 kg of sediment in each. Each microcosm represented a different treatment in terms 101" of biostimulation and/or bioaugmentation. Biostimulation was performed with the addition of 102" N/P in the form of KNO3/ KH2PO4 to a final ratio of C:N:P (100:10:1) while 103" bioaugmentation with the addition of allochthonous bacteria to a final ratio of 10:1 (in terms 104" of CFUs) to the indigenous. The addition of
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