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Altug 06A SC.Docx ACCEPTED MANUSCRIPT 21/07/2020 www.technology.matthey.com Johnson Matthey’s international journal of research exploring science and technology in industrial applications ************Accepted Manuscript*********** This article is an accepted manuscript It has been peer reviewed and accepted for publication but has not yet been copyedited, house styled, proofread or typeset. The final published version may contain differences as a result of the above procedures It will be published in the OCTOBER 2020 issue of the Johnson Matthey Technology Review Please visit the website https://www.technology.matthey.com/ for Open Access to the article and the full issue once published Editorial team Manager Dan Carter Editor Sara Coles Editorial Assistant Yasmin Stephens Senior Information Officer Elisabeth Riley Johnson Matthey Technology Review Johnson Matthey Plc Orchard Road Royston SG8 5HE UK Tel +44 (0)1763 253 000 Email [email protected] Altug_06a_SC.docx ACCEPTED MANUSCRIPT 21/07/2020 Antibiotic and Heavy Metal Resistant Bacteria Isolated From Aegean Sea Water and Sediment in Güllük Bay, Turkey Heavy metal and antibiotic resistant bacteria in Aegean Sea, Turkey Gülşen ALTUĞ* Istanbul University, Faculty of Aquatic Sciences, Department of Marine Biology, Istanbul, Turkey Mine ÇARDAK2 Çanakkale Onsekiz Mart University, Faculty of Çanakkale Applied Sciences, Department of Fisheries Technology, Çanakkale, Turkey Pelin Saliha Çiftçi TÜRETKEN3 Istanbul University, Faculty of Aquatic Sciences, Department of Marine Biology, Istanbul, Turkey Samet KALKAN4 Recep Tayyip Erdoğan University, Faculty of Fisheries, Department of Marine Biology, Rize, Turkey Sevan GÜRÜN1 Istanbul University, Faculty of Aquatic Sciences, Department of Marine Biology, Istanbul, Turkey *Email: [email protected] Johnson Matthey Technol. Rev., 2020, 64, (4), xxx-yyy Page 1 of 45 Doi: 10.1595/205651320X15953337767424 Altug_06a_SC.docx ACCEPTED MANUSCRIPT 21/07/2020 <ABSTRACT> Heavy metal and antibiotic-resistant bacteria have potential for environmental bioremediation applications. Resistant bacteria were investigated in sediment and seawater samples taken from the Aegean Sea, Turkey, between 2011 and 2013. Bioindicator bacteria in seawater samples were tested using the membrane filtration technique. The spread plate technique and VITEC Compact 30 microidentification system were used for heterotrophic aerobic bacteria in the samples. The minimum inhibition concentration method was used for heavy metal-resistant bacteria. Antibiotic-resistant bacteria were tested using the disk diffusion method. All bacteria isolated from sediment samples showed 100% resistance to rifampicin, sulfonamide, tetracycline and ampicillin. 98% of isolates were resistant against nitrofurantoin and oxytetracycline. Higher antibiotic and heavy metal resistance was recorded in bacteria isolated from sediment than seawater samples. The highest levels of bacterial metal resistance were recorded against: copper (58.3%), zinc (33.8%), lead (32.1%), chromium (31%) and iron (25.2%). The results show that antibiotic and heavy metal resistance in bacteria from sediment and seawater can be observed as responses to environmental influences including pollution in marine areas. 1. Introduction In the era of Industry 4.0, with global climate change, increasing population and developing technology, the spread of heavy metal pollutants in aquatic areas is increasing. Bacterial resistance and metal accumulation capability are common phenomena that can be exploited for the bioremediation of the environment, hence these resistant bacteria may be potential candidates for biotechnological applications. Despite the risks caused by antibiotic-resistant bacteria, heavy metal-resistant Johnson Matthey Technol. Rev., 2020, 64, (4), xxx-yyy Page 2 of 45 Doi: 10.1595/205651320X15953337767424 Altug_06a_SC.docx ACCEPTED MANUSCRIPT 21/07/2020 bacteria can be used in detoxification processes to convert a toxic form to a harmless form of a substance by developing biotransformation mechanisms. Bioremediation studies have been carried out to identify candidate species [1–4]. In recent years, the increase in pollution by toxic compounds and heavy metals in marine areas makes it increasingly important to study the relationships between bacteria and toxic compounds. Studies related to the transformation of compounds into different forms via bacterial metabolic processes for the removal of toxic substances from the environment have gained importance. Detection of bacteria that are resistant to heavy metals in natural environments constitutes the first step to provide data for remediation studies. Bacteria are some of the most important components in marine ecosystems. Since bacteria adapt to new conditions created by environmental variables around them, knowledge of bacteria provides data in terms of defining environmental factors, public health status and ecosystem function. Marine areas are exposed to domestic and industrial wastes depending on local technology levels and population. Many xenobiotic micro pollutants, antibiotic derivatives and metabolites reach the sea from human activity. This concerning issue is considered an important factor for global health with respect to the evolution and detection of antibiotic resistance in bacterial pathogens [5]. Since the spread of antimicrobial resistance is not restricted by phylogenetic, geographic or ecological borders, studies describing regional status of bacterial resistance in natural areas are important. Johnson Matthey Technol. Rev., 2020, 64, (4), xxx-yyy Page 3 of 45 Doi: 10.1595/205651320X15953337767424 Altug_06a_SC.docx ACCEPTED MANUSCRIPT 21/07/2020 Antibiotic resistance can spread rapidly among bacterial species [6]. It is known that the occurrence of antibiotic-resistant bacteria in natural environments reduces the effectiveness of antibiotics in the treatment of infectious diseases. Due to the increasing global resistance of bacteria against antibiotics, humanity is constantly being forced to develop new antibiotic derivatives. This vicious circle is one of the most important problems of our age and poses a threat for the future. Thus, it is important to know the resistance levels of bacteria and to produce regional antibiotic resistance profiles in natural areas. Aquatic environments constitute a way to disseminate not only antibiotic-resistant bacteria but also the resistant genes in natural bacterial habitats [7]. It has been well documented that the aquatic environment is a potential reservoir of antibiotic-resistant bacteria, furhermore the prevalence and persistence of antibiotic resistance in bacterial pathogens is a threat and a source of considerable concern to public health [8–15]. It is known that environmental factors such as overpopulation, livestock farming, insufficient drainage and sanitation infrastructure may provide hotspots for environmental antibiotic- resistant bacteria transmission [16]. In aquatic environments, antibiotic-resistant bacteria can be accompanied by heavy metal-resistant bacteria that are often induced by the presence of metal caused by anthropogenic activities and environmental factors [16, 17]. Heavy metals are introduced into the marine environment in different ways. Accumulation in sediment can affect aquatic life negatively for a long time. Bacteria that will take part in the transformation of heavy metal salts into harmless forms must be resistant to the heavy metals. Bacteria that cannot adapt to the changes metabolically will be eliminated and therefore various pollution inputs accumulated in the sediment will Johnson Matthey Technol. Rev., 2020, 64, (4), xxx-yyy Page 4 of 45 Doi: 10.1595/205651320X15953337767424 Altug_06a_SC.docx ACCEPTED MANUSCRIPT 21/07/2020 affect the composition of microbial diversity. Sediments containing harmful, inorganic or organic particles are relatively heterogeneous in terms of physical, chemical, and biological properties and are an important source of heavy metal contamination [11]. It has been reported that microplastics mediate the spread of metal- and antibiotic- resistant pathogens due to their ability to adsorb various pollutants [18, 19]. Bacteria resistant to heavy metals in marine areas have developed various resistance mechanisms to counteract heavy metal stress. Only bacteria that can withstand the current heavy metal concentration can survive in these areas. Heavy metals accumulate in biota via food chains and are transferred between organisms in marine environments. This cumulative process, named biomagnification, is higher in the sea than in terrestrial environments [15, 20] and this implies significant effects of heavy metal pollution in marine areas. On the other hand, heavy metal-resistant bacteria can play a role in detoxification by converting a toxic form into a harmless form through biotransformation mechanisms that develop in natural environments. These mechanisms include the formation and sequestration of heavy metals in complexes and the reduction of a metal to a less toxic species [21, 22]. Metal-resistant bacteria have developed very efficient and varying mechanisms for tolerating high levels of toxic metals and thus they carry an important potential for controlling heavy metal pollution [23]. In many prokaryotes, it has been shown that the mechanism for resisting heavy metals develops over time. This process has been studied in species such as Escherichia coli and Johnson Matthey Technol. Rev., 2020, 64, (4), xxx-yyy Page 5 of 45 Doi: 10.1595/205651320X15953337767424 Altug_06a_SC.docx
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