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Science Journals RESEARCH | REPORTS BIODEGRADATION bers of the filamentous fungi Fusarium oxy- sporum and F. solani, which have been shown to grow on a mineral medium containing PET yarns [although no growth levels were speci- A bacterium that degrades and fied (5, 6)]. Once identified, microorganisms with the enzymatic machinery needed to degrade PET assimilates poly(ethylene terephthalate) could serve as an environmental remediation strategy as well as a degradation and/or fermen- Shosuke Yoshida,1,2* Kazumi Hiraga,1 Toshihiko Takehana,3 Ikuo Taniguchi,4 tation platform for biological recycling of PET Hironao Yamaji,1 Yasuhito Maeda,5 Kiyotsuna Toyohara,5 Kenji Miyamoto,2† waste products. Yoshiharu Kimura,4 Kohei Oda1† We collected 250 PET debris–contaminated en- vironmental samples including sediment, soil, Poly(ethylene terephthalate) (PET) is used extensively worldwide in plastic products, and its wastewater, and activated sludge from a PET accumulation in the environment has become a global concern. Because the ability to bottle recycling site (7). Using these samples, enzymatically degrade PET has been thought to be limited to a few fungal species, we screened for microorganisms that could use biodegradation is not yet a viable remediation or recycling strategy. By screening natural low-crystallinity (1.9%) PET film as the major microbial communities exposed to PET in the environment, we isolated a novel bacterium, carbon source for growth. One sediment sample Ideonella sakaiensis 201-F6, that is able to use PET as its major energy and carbon source. contained a distinct microbial consortium that When grown on PET, this strain produces two enzymes capable of hydrolyzing PET and the formed on the PET film upon culturing (Fig. 1A) reaction intermediate, mono(2-hydroxyethyl) terephthalic acid. Both enzymes are required to and induced morphological change in the PET enzymatically convert PET efficiently into its two environmentally benign monomers, film (Fig. 1B). Microscopy revealed that the con- terephthalic acid and ethylene glycol. sortium on the film, termed “no. 46,” contained lastics with desirable properties such as degradation (2, 3). About 56 million tons of PET 1Department of Applied Biology, Faculty of Textile Science, durability, plasticity, and/or transparency was produced worldwide in 2013 alone, prompt- Kyoto Institute of Technology, Matsugasaki, Sakyo-ku, Kyoto 606-8585, Japan. 2Department of Biosciences and have been industrially produced over the ing further industrial production of its mono- Informatics, Keio University, 3-14-1 Hiyoshi, Kohoku-ku, past century and widely incorporated into mers, terephthalic acid (TPA) and ethylene glycol Yokohama, Kanagawa 223-8522, Japan. 3Life Science P Materials Laboratory, ADEKA, 7-2-34 Higashiogu, Arakawa-ku, consumer products (1). Many of these pro- (EG), both of which are derived from raw petro- 4 ducts are remarkably persistent in the environ- leum. Large quantities of PET have been intro- Tokyo 116-8553, Japan. Department of Polymer Science, Faculty of Textile Science, Kyoto Institute of Technology, ment because of the absence or low activity of duced into the environment through its production Matsugasaki, Sakyo-ku, Kyoto 606-8585, Japan. 5Ecology- catabolic enzymes that can break down their and disposal, resulting in the accumulation of PET Related Material Group Innovation Research Institute, Teijin, on March 10, 2016 plastic constituents. In particular, polyesters con- in ecosystems across the globe (4). Hinode-cho 2-1, Iwakuni, Yamaguchi 740-8511, Japan. taining a high ratio of aromatic components, such There are very few reports on the biological *Present address: Department of Polymer Chemistry, Graduate School of Engineering, Kyoto University, Nishikyo-ku, Kyoto 615- as poly(ethylene terephthalate) (PET), are chem- degradation of PET or its utilization to support 8530, Japan. †Corresponding author. E-mail: kmiyamoto@bio. ically inert, resulting in resistance to microbial microbial growth. Rare examples include mem- keio.ac.jp (K.M.); [email protected] (K.O.) 0 Downloaded from 10 20 30 40 50 Weight loss (mg) Weight loss PET 60 film 020406080 Cultivation time (days) 1 1 2 3 2 0 6 10 3 20 4 4 6 30 5 5 40 50 Weight loss (mg) 8 7 8 60 7 0204060 910 9 10 Cultivation time (days) Fig. 1. Microbial growth on PET. The degradation of PET film (60 mg, 20 × vitamins) medium was changed weekly. (D to F) SEM images of I. sakaiensis 15 × 0.2 mm) by microbial consortium no. 46 at 30°C is shown in (A) to (C). cells grown on PET film for 60 hours. Scale bars, 1 mm. Arrow heads in the left The MLE (modified lettuce and egg) medium (10 mL) was changed biweekly. panel of (D) indicate contact points of cell appendages and the PET film surface. (A) Growth of no. 46 on PET film after 20 days. (B) SEM image of degraded PET Magnifications are shown in the right panel. Arrows in (F) indicate appendages film after 70 days. The inset shows intact PET film. Scale bar, 0.5 mm. (C)Time between the cell and the PET film surface. (G) SEM image of a degraded PET course of PET film degradation by no. 46. PET film degradation by I. sakaiensis film surface after washing out adherent cells. The inset shows intact PET film. 201-F6 at 30°C is shown in (D) to (H).The YSV (yeast extract–sodium carbonate– Scale bar, 1 mm. (H) Time course of PET film degradation by I. sakaiensis. 1196 11 MARCH 2016 • VOL 351 ISSUE 6278 sciencemag.org SCIENCE RESEARCH | REPORTS a mixture of bacteria, yeast-like cells, and proto- Biotechnology Information taxonomy database There are currently few known examples of zoa, whereas the culture fluid was almost trans- under identifier 1547922). In addition to being esterases, lipases, or cutinases that are capable parent (Fig. 1A). This consortium degraded the found in the culture fluid, cells were observed on of hydrolyzing PET (8, 9). To explore the genes PET film surface (fig. S1) at a rate of 0.13 mg cm–2 the film (Fig. 1D) and appeared to be connected involved in PET hydrolysis in I. sakaiensis 201- day–1 at30°C(Fig.1C),and75%ofthedegraded to each other by appendages (Fig. 1E). Shorter F6, we assembled a draft sequence of its genome PET film carbon was catabolized into CO2 at 28°C appendages were observed between the cells and (table S1). One identified open reading frame (fig. S2). the film; these might assist in the delivery of se- (ORF), ISF6_4831, encodes a putative lipase that Using limiting dilutions of consortium no. 46 creted enzymes into the film (Fig. 1, D and F). shares 51% amino acid sequence identity and that were cultured with PET film to enrich for The PET film was damaged extensively (Fig. 1G) catalytic residues with a hydrolase from Ther- microorganisms that are nutritionally dependent and almost completely degraded after 6 weeks at mobifida fusca (TfH) (fig. S4 and table S2) that on PET, we successfully isolated a bacterium capa- 30°C(Fig.1H).Inthecourseofsubculturingno. exhibits PET-hydrolytic activity (10). We purified the ble of degrading and assimilating PET. The strain 46, we found a subconsortium that lost its PET corresponding recombinant I. sakaiensis proteins represents a novel species of the genus Ideonella, degradation capability. This subconsortium lacked (fig. S5) and incubated them with PET film at for which we propose the name Ideonella sakaiensis I. sakaiensis (fig. S3), indicating that I. sakaiensis 30°C for 18 hours. Prominent pitting developed on 201-F6 (deposited in the National Center for is functionally involved in PET degradation. the film surface (Fig. 2A). Mono(2-hydroxyethyl) Thermobifida group 4OYY ADV92528 TfH (Humicola insolens) (T. fusca) ADV92526 ADV92527 (T. cellulosilytica) (T. cellulosilytica) 991ADV92525 AFA45122.1 982 997 (T. halotolerans) (T. alba) 1000 BAO42836.1 668 (Saccharomonospora viridis) 1000 1000 FsC 986 1000 MHET O O HO OH CH2 CH2 O C C LCCLCC O O HO C C OH TPA BHET O O HO CH2 CH2 O C C O CH2 CH2 OH 10 mV PETase 18h 0h 0.1 18 19 20 21 22 23 24 ADH43200.1 Retention time (min) (Bacillus subtilis) pNP-aliphatic esters (a) PET-film (b) b/a BHET hcPET 10 pNP-acetate (C2) PETase pNP-butyrate (C4) pNP-caproate (C6) 100 LLCCCC pNP-caprylate (C8) PETase PETase TfH 10-1 TfH -2 TfH LCCLCC 10 LCCLCC TPA b/a(C2) b/a(C4) MHET TPA 10-3 b/a(C6) FsC FsC BHET MHET b/a(C8) FsC Total released compounds (mM) 10-4 040801200 0.1 0.2 0.3 -5 -4 -3 -2 -1 0 00.80.4 00.010 0.005 0.015 20 30 40 50 60 70 80 -1 -1 Apparent kcat (sec ) Released compounds (mM) log10Ratio Apparent kcat (sec ) Released compounds (mM) Temperature (°C) Fig. 2. ISF6_4831 protein is a PETase. Effects of PETase on PET film are panel to those in the leftmost panel). All reactions were performed in pH shown in (A) and (B). PET film (diameter, 6 mm) was incubated with 50 nM 7.0 buffer at 30°C. PET film was incubated with 50 nM enzyme for 18 hours. PETase in pH 7.0 buffer for 18 hours at 30°C. (A) SEM image of the treated (E) Activity of the PET hydrolytic enzymes for highly crystallized PET PET film surface. The inset shows intact PET film. Scale bar, 5 mm. (B)High- (hcPET). The hcPET (diameter, 6 mm) was incubated with 50 nM PETase performance liquid chromatography spectrum of the products released from or 200 nM TfH, LCC, or FsC in pH 9.0 bicine-NaOH buffer for 18 hours at the PET film. (C) Unrooted phylogenetic tree of known PET hydrolytic en- 30°C. (F) Effect of temperature on enzymatic PET film hydrolysis.
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