The plastisphere in marine ecosystem hosts potential specific microbial degraders including Alcanivorax borkumensis as a key player for the low-density polyethylene degradation
[en] Most plastics are released to the environment in landfills and around 32% end up in the sea, inducing large ecological and health impacts. The plastics constitute a physical substrate and potential carbon source for microorganisms. The present study compares the structures of bacterial communities from floating plastics, sediment-associated plastics and sediments from the Mediterranean Sea. The 16S rRNA microbiome profiles of surface and sediment plastic-associated microbial biofilms from the same geographic location differ significantly, with the omnipresence of Bacteroidetes and Gammaproteobacteria. Our research confirmed that plastisphere hosts microbial communities were environmental distinct niche. In parallel, this study used environmental samples to investigate the enrichment of potential plastic-degrading bacteria with Low Density PolyEthylene (LDPE), PolyEthylene Terephthalate (PET) and PolyStyrene (PS) plastics as the sole carbon source. In this context, we showed that the bacterial community composition is clearly plastic nature dependent. Hydrocarbon-degrading bacteria such as Alcanivorax, Marinobacter and Arenibacter genera are enriched with LDPE and PET, implying that these bacteria are potential players in plastic degradation. Finally, our data showed for the first time the ability of Alcanivorax borkumensis to form thick biofilms specifically on LDPE and to degrade this petroleum-based plastic.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège Stareso
Delacuvellerie, Alice; Proteomics and Microbiology Department, University of Mons, 20 place du Parc, Mons, 7000, Belgium
Cyriaque, Valentine; Proteomics and Microbiology Department, University of Mons, 20 place du Parc, Mons, 7000, Belgium
Gobert, Sylvie ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Benali, Samira; Polymer and Composite Materials Department, University of Mons, 15 Avenue Maistriau, Mons, 7000, Belgium
Wattiez, Ruddy; Proteomics and Microbiology Department, University of Mons, 20 place du Parc, Mons, 7000, Belgium
Language :
English
Title :
The plastisphere in marine ecosystem hosts potential specific microbial degraders including Alcanivorax borkumensis as a key player for the low-density polyethylene degradation
Publication date :
2019
Journal title :
Journal of Hazardous Materials
ISSN :
0304-3894
eISSN :
1873-3336
Publisher :
Elsevier B.V.
Volume :
380
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
UMONS - Université de Mons F.R.S.-FNRS - Fund for Scientific Research
Funding number :
Fund for Scientific Research (F.R.S-FNRS) FC 23347
Alomar, C., Deudero, S., Evidence of microplastic ingestion in the shark Galeus melastomus Rafinesque, 1810 in the continental shelf off the western Mediterranean Sea. Environ. Pollut.(223), 2017, 223–229.
Andrady, A.L., Microplastics in the marine environment. Mar. Pollut. Bull. 62 (2011), 1596–1605.
Artham, T., Doble, M., Biodegradation of aliphatic and aromatic polycarbonates. Macromol. Biosci. 8:1 (2008), 14–24.
Bauer, M., Kube, M., Teeling, H., Richter, M., Lombardot, T., Allers, E., et al. Whole genome analysis of the marine Bacteroidetes “Gramella forsetii” reveals adaptations to degradation of polymeric organic matter. Environ. Microbiol. 8 (2006), 2201–2213.
Boren, L.J., Morrissey, M., Muller, C.G., Gemmell, N.J., Entanglement of New Zealand fur seals in man-made debris at Kaikoura, New Zealand. Mar. Pollut. Bull. 52 (2006), 442–446.
Bryant, J.A., Clemente, T.M., Viviani, D.A., Fong, A.A., Thomas, K.A., Kemp, P., Karl, D.M., White, A.E., DeLong, E.F., Diversity and activity of communities inhabiting plastic debris in the north pacific gyre. mSystems 1:3 (2016), e00024–16.
De Tender, C.A., Devriese, L.I., Haegeman, A., Maes, S., Ruttink, T., Dawyndt, P., Bacterial community profiling of plastic litter in the Belgian part of the North Sea. Environ. Sci. Technol. 49 (2015), 9629–9638.
De Tender, C.A., Devriese, L.I., Haegeman, A., Maes, S., vangeyte, J., Cattrijsse, A., Dawyndt, P., Ruttink, T., The temporal dynamics of bacterial and fungal colonization on plastic debris in the North Sea. Environ. Sci. Technol. 49 (2017), 9629–9638.
De Tender, C., Schlundt, C., Devriese, L.I., Mincer, T.J., Zettler, E.R., Amaral-Zettler, L.A., A review of microscopy and comparative molecular-based methods to characterize “Plastisphere” communities. Anal. Methods 9 (2017), 2132–2143.
Debroas, D., Mone, A., TerHalle, A., Plastics in the North Atlantic garbage patch: a boat-microbe for hitchhikers and plastic degraders. Sci. Total Environ. 599-600 (2017), 1222–1232.
Dixon, P., VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14 (2003), 927–930.
Ellen MacArthur Foundation, The New Plastics Economy: Rethinking the Future of Plastics. 2016, 120.
Galgani, F., Leaute, J.P., Moguedet, P., Souplet, A., Verin, Y., Carpentier, A., Goraguer, H., Latrouite, D., Litter on the sea floor along European coasts. Mar. Pollut. Bull. 40:6 (2000), 516–527.
Gauthier, M.J., Lafay, B., Christen, R., Fernandez, L., Acquaviva, M., Bonin, P., Bertrand, J.C., Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int. J. Syst. Bacteriol. 42:4 (1992), 568–576.
Gilan, I., Hadar, Y., Sivan, A., Colonization, biofilm formation and biodegradation of polyethylene by a strain of Rhodococcus ruber. Appl. Microbiol. Biotechnol. 65 (2004), 97–104.
Golyshin, P.N., Martins Dos Santos, V.A.P., Kaiser, O., Ferrer, M., Sabirova, Y.S., Lünsdorf, H., Chernikova, T.N., Golyshina, O.V., Yakimov, M.M., Pühler, A., Timmis, K.N., Genome sequence completed of Alcanivorax borkumensis a hydrocarbon-degrading bacterium that plays a global role in oil removal from marine systems. J. Biotechnol. 106 (2003), 215–220.
Gutierrez, T., Whitman, W.B., Huntemann, M., Copeland, A., Chen, A., Kyrpides, N., Markowitz, V., Pillay, M., Ivanova, N., Mikhailova, N., Ovchinnikova, G., et al. Genome sequence of Arenibacter algicola strain TG409, a hydrocarbon-degrading bacterium associated with marine eukaryotic phytoplankton. Genome Announc. 4:4 (2016), e00765–16.
Güven, O., Gökdag, K., Jovanovic, B., Kideys, A.E., Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ. Pollut. 223 (2017), 286–294.
Hajighasemi, M., Nocek, B.P., Tchigvintsev, A., Brown, G., Hai, T., Joachimiak, A., Golyshin, P.N., Savchenko, A., Edwards, E.A., Yakunin, A.F., Biochimical and structural insights into enzymatic depolymerization of polylactic acid and other polyesters by microbial carboxylesterases. Biomacromolecules 17:6 (2016), 2027–2039.
Hammer, Ø., Harper, D.A.T., Ryan, P.D., Paleontological statistics software package for education and data analysis. Palaeontol. Electronica 4:1 (2001), 9–18.
Harrison, J.P., Schratzberger, M., Sapp, M., Osborn, A.M., Rapid bacterial colonization of low-density polyethylene microplastics in coastal sediment microcosmes. BMC Microbiol., 2014, 14–232.
Hollein, T., Rojas, M., Pink, A., Gasior, J., Kelly, J., Anthropogenic litter in urban freshwater ecosystems: distribution and microbial interactions. PLoS One, 9(6), 2014.
Jacquiod, S., Cyriaque, V., Riber, L., Abu Al-soud, W., Gillan, C.G., Wattiez, R., Sorensen, S.J., Long-term industrial metal contamination unexpectedly shaped diversity and activity response of sediment microbiome. J. Hazardous Mater., 344, 2018 29kolter-307.
Jiang, P., Zhao, S., Zhu, L., Li, D., Microplastic-associated bacterial assemblages in the intertidal zone of the Yangtze Estuary. Sci. Total Environ. 624 (2018), 48–54.
Kalenitchenko, D., Fagervold, S.K., Pruski, A.M., Vétion, G., Yüel, M., Le Bris, N., Galand, P.E., Temporal and spatial constraints on community assembly during microbial colonization of wood in seawater. ISME J. 9 (2015), 2657–2670.
Kirstein, V.I., Kirmizia, S., Wichelsa, A., Garin-Fernandez, A., Erler, R., Löder, M., Gerdts, G., Dangerous hitchhikers? Evidence for potentially pathogenic Vibrio spp. On microplastic particles. Mar. Environ. Res. 120 (2016), 1–8.
Klippel, B., Lochner, A., Bruce, D., Walston Davenport, K., Detter, C., Goodwin, L.A., Han, J., Han, S., Land, M.L., Mirkhailova, N., Nolan, M., et al. Complete genome sequence of the marine cellulose- and xylan-degrading bacterium Glaciecola sp. Strain 4H-3-7+YE-5. J. Bacteriol. 193:17 (2011), 4547–4548.
Konieczna, M., Olzog, M., Naether, D.J., Chrzanowski, Ł., Heipieper, H.J., Membrane fatty acid composition and cell surface hydrophobicity of marine hydrocarbonoclastic Alcanivorax borkumensis SK2 grown on diesel, biodiesel and rapeseed oil as carbon sources. Molecules, 23(6), 2018.
Kühn, S., Bravo Rebolledo, E.L., van Franeker, J.A., Deleterious effects of litter on Marine life. Bergmann, M., Gutow, L., Klages, M., (eds.) Marine Anthropogenic Litter, 2015, Springer, Cham.
Lehner, A., Tasara, T., Stephan, R., Relevant aspects of Arcobacter spp. As potential foodborne pathogen. Int. J. Food Microbiol. 102:2 (2005), 127–135.
Li, H., Liu, Y.H., Luo, N., Zhang, X.Y., Luan, T.G., Hu, J.M., Wang, Z.Y., Wu, P.C., Chen, M.J., Lu, J.Q., Biodegradation of benzene and its derivatives by a psychrotolerant and moderately haloalkaliphilic Planococcus sp. Strain ZD22. Res. Microbiol. 157 (2006), 629–636.
Lyche, J.L., Gutleb, A.C., Bergman, A., Eriksen, G.S., Murk, A.J., Ropstad, E., Saunders, M., Skaare, J.U., Reproductive and developmental toxicity of phthalates. J. Toxicol. Environ. Health 12 (2009), 225–249.
Mahoney, K.W., Talbert, J.N., Goddard, J.M., Effect of polyethylene glycol tether size and chemistry on the attachment of lactase to polyethylene films. J. Appl. Polym. Sci. 127:2 (2013), 1203–1210.
Melcher, R.J., Apitz, S.E., Hemmingsen, B.B., Impact of irradiation and polycyclic aromatic hydrocarbon spiking on microbial populations in marine sediment for future aging and biodegradability studies. Appl. Environ. Microbiol. 68 (2002), 2858–2868.
Mor, R., Sivan, A., Biofilm Formation and Partial Biodegradation of Polystyrene by the Actinomycete Rhodococcus ruber, 19, 2008, Springer, 851–858.
Morét-Ferguson, S., Law, K.L., Proskurowski, G., Murphy, E.K., Peacock, E.E., Reddy, C.M., The size, mass, and composition of plastic debris in the western North Atlantic Ocean. Mar. Pollut. Bull. 60 (2010), 1873–1878.
Muhonja1, C.N., Makonde, H., Magoma1, G., Imbuga, M., Biodegradability of polyethylene by bacteria and fungi from Dandora dumpsite Nairobi Kenya. PLoS One, 13(7), 2018.
Munari, C., Scoponi, M., Mistri, M., Plastic debris in the Mediterranean Sea: types, occurrence and distribution along Adriatic shorelines. Waste Manage. 67 (2017), 385–391.
Naether, D.J., Slawtschew, S., Stasik, S., Engel, M., Olzog, M., Wick, L.Y., Timmis, K.N., Heipieper, J.H., Adaptation of the hydrocarbonoclastic Bacterium Alcanivorax borkumensis SK2 to alkanes and toxic organic compounds: a physiological and transcriptomic approach. Appl. Environ. Microbiol. 79:14 (2013), 4282–4293.
Newton, R.J., Huse, S.M., Morrison, H.G., Peake, C.S., Sogin, M.L., McLellan, S.L., Shifts in the microbial community composition of gulf coast beaches following beach oiling. PLoS One, 9(4), 2013, e94671.
Noh, J., Kim, H., Lee, C., Yoon, S.J., Chu, S., Kwon, B.O., Ryu, J., Kim, J.J., Lee, H., Yim, U.H., Giesy, J.P., Khim, J.S., Bioaccumulation of Polycyclic Aromatic Hydrocarbons (PAHs) by the Marine Clam, Mactra veneriformis, chronically exposed to oil-suspended particulate matter aggregates. Environ. Sci. Technol. 52:14 (2018), 7910–7920.
Nunes, I., Jacquiod, S., Brejnrod, A., Holm, P.E., Johansen, A., Brandt, K.K., Priemé, A., Sorensen, S.J., Coping with copper: legacy effect of copper on potential activity of soil bacteria following a century of exposure. FEMS Microb. Ecol., 92(11), 2016.
O'Toole, G.A., Kolter, R., Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28 (1998), 449–461.
Oberbeckmann, S., Osborn, A.M., Duhaime, M.B., Microbes on a bottle: substrate, season and geography influence community composition of microbes colonizing marine plastic debris. PLoS One, 11(8), 2016, e0159289.
Oberbeckmann, S., Loeder, M.G.J., Gerdts, G., Osborn, A.M., Spatial and seasonal variation in diversity and structure of microbial biofilms on marine plastics in Northern European waters. Microbiol. Ecol. 90 (2014), 478–492.
Pathak, M.P., Navneet, Review on the current status of polymer degradation: a microbial approach. Bioresour. Bioprocess., 4(15), 2017.
PlasticsEurope, Plastics – The Facts 2017 an Analysis of European Plastics Production Demand and Waste Data. 2017.
Polymenakou, P.N., Bertilsson, S., Tselepides, A., Stephanou, E.G., Bacterial community composition in different sediments from the Eastern Mediterranean Sea: a comparison of four 16S ribosomal DNA clone libraries. Microb. Ecol. 50 (2005), 447–462.
Polz, M.F., Hunt, D.E., Preheim, S.P., Weinreich, D.M., Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes. Philos. Trans. Biol. Sci. 361 (2006), 2009–2021.
Poon, F., Provencher, J.F., Mallory, M.L., Braune, B.M., Smith, P., Levels of ingested debris vary across species in Canadian Arctic seabirds. Mar. Pollut. Bull. 116:1-2 (2017), 517–520.
Prince, R.C., Gramain, A., McGenity, T.J., Prokaryotic hydrocarbon degraders. Timmis, K.N., (eds.) Handbook of Hydrocarbon and Lipid Microbiology, 2010, Springer, Berlin, Heidelberg.
Rios, L.M., Moore, C., Jones, P.R., Persistent organic pollutants carried by synthetic polymers in the ocean environment. Mar. Pollut. Bull. 54:8 (2007), 1230–1237.
Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W., Smyth, G.K., Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, 2015, e47.
Rochester, J.R., Bisphenol A and human health: a review of the literature. Reprod. Toxicol. 42 (2013), 132–155.
Sabirova, J.S., Becker, A., Lünsdorf, H., Nicaud, J.-M., Timmis, K.N., Golyshin, P.N., Transcriptional profiling of the marine oil-degrading bacterium Alcanivorax borkumensis during growth n-alkanes. FEMS Microbiol. Lett. 319 (2011), 160–168.
Shannon, P., Markiel, A., Ozier, O., Balig, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., Ideker, T., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13 (2003), 2498–2504.
Skariyachan, S., Manjunatha, V., Sultana, S., Jois, C., Bai, V., Vasist, K.S., Novel bacterial consortia isolated from plastic garbage processing areas demonstrated enhanced degradation for low density polyethylene. Environ. Sci. Pollut. Res 23:18 (2016), 18307–18319.
Skariyachan, S., Setlur, A.S., Naik, S.Y., Naik, A.A., Usharani, M., Vasist, K.S., Enhanced biodegradation of low and high-density polyethylene by novel bacterial consortia formulated from plastic-contaminated cow dung under thermophilic conditions. Environ. Sci. Pollut. Res. 24:9 (2017), 8443–8457.
Sudhakar, M., Doble, M., Murthy, P.S., Venkatesan, R., Marine microbe-mediated biodegradation of low- and high-density polyethylenes. Int. Biodeterior. Biodegrad. 61:3 (2008), 203–213.
Teramoto, M., Ohuchi, M., Hatmanti, A., Darmayati, Y., Widyastuti, Y., Harayama, S., Fukunaga, Y., Oleibacter marinus gen. nov., sp. Nov., a bacterium that degrades petroleum aliphatic hydrocarbons in a tropical marine environment. Int. J. Syst. Evol. Microbiol. 61 (2011), 375–380.
Ulitzur, S., Vibrio parahaemolyticus and Vibrio alginolyticus. Short generation- time marine Bacteria. Microb. Ecol. 1 (1974), 127–135.
Van der Hal, N., Ariel, A., Anger, D.L., Exceptionally high abundances of microplastics in the oligotrophic Israeli Mediterranean coastal waters. Mar. Pollut. Bull. 116 (2017), 151–155.
Wang, Y., Naumann, U., Wright, S.T., Warton, D.I., Mvabund – an R package for model-based analysis of multivariate abundance data. Methods Ecol. Evol. 3 (2012), 471–474.
Wilkes, R.A., Aristilde, L., Degradation and metabolism of synthetic plastics and associated products by Pseudomonas sp.: capabilities and challenges. J. Appl. Microbiol. 123:3 (2017), 582–593.
Woodall, L.C., Sanchez-vidal, A., Paterson, G.L.J., Coppock, R., Sleight, V., Calafat, A., Rogers, A.D., Narayanaswamy, B.E., Thompson, R.C., The deep sea is a major sink for microplastic debris. R. Soc. Open Sci., 1, 2014, 140371.
Yakimov, M.M., Golyshin, P.N., Lang, S., Moore, E.R., Abraham, W.R., Lunsdorf, H., Timmis, K.N., Alcanivorax borkumensis gen., nov., sp., nov., a new hydrocarbon-degrading and surfactant-producing marine bacterium. Int. J. Syst. Bacteriol. 48 (1998), 339–348.
Yang, Y., Yang, J., Wu, W., Zhao, J., Song, Y., Gao, L., Yang, R., Jiang, L., Biodegradation and mineralization of polystyrene by plastic-eating mealworms: part 2. role of gut microorganisms. Environ. Sci. Technol. 49 (2015), 12087–12093.
Yoshida, S., Hiraga, K., Takehana, T., Taniguchi, I., Yamaji, H., Maeda, Y., Toyohara, K., Miyamoto, K., Kimura, Y., Oda, K., A bacterium that degrades and assimilates poly(ethyleneterephthalate). Science 351 (2016), 1196–1199.
Zettler, E.R., Mincer, T.J., Amaral-Zettler, L.A., Life in the “Plastisphere”: microbial communities on plastics marine debris. Environ. Sci. Technol. 47:13 (2013), 7137–7146.