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Biofilm Formation by Exiguobacterium Sp. DR11 and DR14 Alter Polystyrene Surface Properties and Initiate Biodegradation

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Biofilm Formation by Exiguobacterium Sp. DR11 and DR14 Alter Polystyrene Surface Properties and Initiate Biodegradation RSC Advances View Article Online PAPER View Journal | View Issue Biofilm formation by Exiguobacterium sp. DR11 and DR14 alter polystyrene surface properties and Cite this: RSC Adv.,2018,8,37590 initiate biodegradation† Deepika Chauhan,a Guncha Agrawal,a Sujit Deshmukh,b Susanta Sinha Royb and Richa Priyadarshini *a Polystyrene is a chemically inert synthetic aromatic polymer. This widely used form of plastic is recalcitrant to biodegradation. The exponential production and consumption of polystyrene in various sectors has presented a great environment risk and raised the problem of waste management. Biodegradation by bacteria has previously shown great potential against various xenobiotics but there are only a few reports concerning polyolefins. By screening wetland microbes, we found two bacterial species – Exiguobacterium sibiricum strain DR11 and Exiguobacterium undae strain DR14 which showed promising biodegradation potential against polystyrene. In this study, we report the degradation of non-irradiated solid polystyrene material Creative Commons Attribution-NonCommercial 3.0 Unported Licence. after incubation with these isolates. Growth studies suggested that the Exiguobacterium strains utilize polystyrene as a carbon source. Moreover, our data suggest that polymer degradation was initiated by biofilm formation over the PS surface leading to alteration in the physical properties of the material. Surface property analysis by AFM revealed significantly enhanced roughness resulting in reduced surface hydrophobicity of polystyrene. Fourier-transfer infrared (FT-IR) spectroscopic analysis showed breakdown Received 31st July 2018 of polystyrene backbone by oxidation. The extent of deterioration was further determined by percent Accepted 1st November 2018 weight reduction of polystyrene after incubation with bacteria. Our data support the fact that strains of DOI: 10.1039/c8ra06448b extremophile bacterium Exiguobacterium are capable of degrading polystyrene and can be further used to rsc.li/rsc-advances mitigate the environmental pollution caused by plastics. This article is licensed under a 1. Introduction nature of plastic poses a severe environmental hazard. PS is also a major terrestrial and marine pollutant.6–9 Open Access Article. Published on 08 November 2018. Downloaded 9/25/2021 4:03:37 AM. Over the years plastic or synthetic polymers have been deeply Polymer degradation is dened as the conversion of polymer incorporated into human life. Their high durability, resistance into smaller subunits by breaking bonds through physical, to change in temperature, light weight and low cost have made chemical or biological processes leading to alteration in the plastic a material of choice in each sector.1,2 Among the most physico-chemical properties of the polymer. A few alternative widely used forms of polyolens, polyethylene (PE), poly- abiotic processes are also known to play a role in polymer propylene (PP) and polystyrene (PS) are majorly used in the degradation. These include thermal, photo-oxidative, ozone- packaging industry.3 PS is a synthetic aromatic polymer based degradation, catalytic and mechanochemical methods.10 synthesized by polymerization of styrene units. The expanded Exposure to sunlight/UV-radiation has been reported to enhance form of PS is styrofoam, and it is commonly used as a packaging the chain breakage in PS structure initiating degradation process. material and for manufacturing disposable cups and cutlery, As an alternative to the conventional methods of polymer containers and laboratory consumables.4 Because of the exten- degradation, biodegradation presents itself as an economic and sive use and increasing demand, annual production of PS has environment-friendly approach. Biodegradation is a complex crossed the scale of several million tonnes.5 The recalcitrant process of physico-chemical transformation of polymers into smaller units by the action of microorganisms. It is a relatively slow process in which cleavage of polymer backbone by bond scission leads to generation of carbonyl groups (oxidation) which aDepartment of Life Sciences, School of Natural Sciences, Shiv Nadar University, are considered to be utilized by the microorganism as a source of Gautam Buddha Nagar, Uttar Pradesh, India. E-mail: [email protected]. carbon and energy.11–13 There are a few reports showing biodeg- in; Tel: +91-120-3819100 ext. 220 radation of synthetic polymers including polyethylene, poly- bDepartment of Physics, School of Natural Sciences, Shiv Nadar University, Gautam urethane, polyvinyl chloride14–20 and their microplastic forms.21–23 Buddha Nagar, Uttar Pradesh, India † Electronic supplementary information (ESI) available. See DOI: PS also belongs to a non-biodegradable class of synthetic poly- 12 10.1039/c8ra06448b mers but very limited data is available on its biodegradation. 37590 | RSC Adv.,2018,8,37590–37599 This journal is © The Royal Society of Chemistry 2018 View Article Online Paper RSC Advances The monomeric form, styrene, has been studied and has shown 2.2 Bacterial strains and culture conditions degradable properties.24–27 It is considered that to initiate the For initial screening and isolation NB, LB and TSB were process of PS biodegradation, prior exposure to photo-oxidation selected. Nutrient agar (NA) and skim milk agar (SMA) (Himedia and thermal induction is required. This, in turn, causes bond Pvt. Ltd., India) was used for motility and proteolytic assays scission and formation of new functional groups.28,29 respectively. Aer identication for subsequent experiments In nature, bacteria exist in sessile communities known as Exiguobacterium sp. strain DR11 and Exiguobacterium sp. strain biolms. Biolms provide protection from harsh environmental DR14 were grown in nutrient broth (NB) on a shaking incubator 30,31 conditions and resistance to chemical stress. Studies show (200 rpm) at 30 C. To detect the activity of PS degradation, that biodegradation by microbial bio lms is more favourable liquid carbon-free basal medium (LCFBM) was used containing 32 than planktonic bacteria. Initial adherence of bacteria on the À1 $ (g l ): 0.7 g of KH2PO4, 0.7 g of K2HPO4, 0.7 g of MgSO4 7H2O, surface of plastics is followed by the colonization of the exposed 1.0 g of NH4NO3, 0.005 g of NaCl, 0.002 g of FeSO4$7H2O, plastic surface. It is proposed that initiation of biolms 37 0.002 g of ZnSO4$7H2O, and 0.001 g of MnSO4$H2O. enhances carbon utilization from non-soluble substrates such as PS and PE. Biodegradation of polymer is achieved by two 2.3 Identication of bacterial species types of enzymes intracellular and extracellular depolymerases. The extracellular depolymerases secreted from microorganisms For identication, DNA was isolated conventionally and then convert the polymers into monomers, dimers or oligomers 16S rRNA gene sequence was amplied by PCR using universal 0 0 which can permeate through bacterial cell membrane and are primers: 27F – (5 -AGAGTTTGATCMTGGCTCAG-3 ) and 1492R – 0 0 utilized as a source of carbon and energy. (5 -TACGGYTACCTTGTTACGACTT-3 ). PCR reaction mixture Biodiversity and occurrence of polymer-degrading microor- containing Taq polymerase (NEB) was set under the following ganisms show variation depending on the ecological habitat, cycling conditions: 94 C for 10 min, (94 C for 40 s, 56 C for such as soil, water, compost, or sludge. Wetlands are one of the 1 min, 74 C for 2 min) X30 cycles, 74 C for 10 min using Eppendorf thermal master cycler (Eppendorf, Hamburg, Ger- Creative Commons Attribution-NonCommercial 3.0 Unported Licence. richest habitats of microbial diversity as they provide complex as well as distinct environmental conditions.33 These ecosys- many). PCR amplied products were puried using PCR puri- tems are ideal grounds for isolating bacteria with novel cation kit (Qiagen India Pvt Ltd) and sent for sequencing enzymes. Members of Exiguobacterium genus are considered (SciGenom Labs Pvt Ltd, Kerala, India). The sequence similarity extremophiles as they possess extreme tolerance to temperature was veried by using basic local alignment search tool (BLAST) (À12 Cto55C), halo tolerance (up to 13%) and can grow in on NCBI (http://www.ncbi.nlm.nih.gov/). Sequences of both the a wide range of pH (5–11). These rmicutes thrive in most isolates, Exiguobacterium sp. strain DR11 and DR14, have been extreme environments such as ancient Siberian permafrost and submitted in the NCBI (Genbank accession ID numbers – hot springs to freshwater ecosystem.34–36 Yet, only one study MG645229, MG645233 respectively). Both the strains are This article is licensed under a reported the role of Exiguobacterium sp. strain YT2 in PS publically deposited in Microbial Type Culture Collection degradation which was isolated from the gut of a mealworm.37 (MTCC 12887, 12888), Chandigarh, India and are available for In this study, we are reporting initiation of PS degradation by public use. Exiguobacterium sp. strains DR11 and DR14 isolated from Dadri Open Access Article. Published on 08 November 2018. Downloaded 9/25/2021 4:03:37 AM. wetlands, India. PS degradation by Exiguobacterium sp. strains 2.4 Polystyrene material DR11 and DR14 was veried by analysis of various parameters Two types of PS material were used for this study including (1 Â such as FT-IR analysis, hydrophobicity test and AFM imaging. 1) cm cut pieces of optically clear, sterile polystyrene Petri We are also reporting biolm formation over the PS surface by plates, 90 mm (Himedia Lab Pvt Ltd, Mumbai, India) and PS the
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