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Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 30067–30083 | Cite as

Effects of microplastics on trophic parameters, abundance and metabolic activities of seawater and fish gut bacteria in mesocosm conditions

  • Gabriella Caruso
  • Cristina Pedà
  • Simone Cappello
  • Marcella Leonardi
  • Rosabruna La Ferla
  • Angelina Lo Giudice
  • Giulia Maricchiolo
  • Carmen Rizzo
  • Giovanna Maimone
  • Alessandro Ciro Rappazzo
  • Lucrezia Genovese
  • Teresa Romeo
Research Article

Abstract

Plastic pollution is an emerging threat with severe implications on animals’ and environmental health. Nevertheless, interactions of plastic particles with both microbial structure and metabolism are a new research challenge that needs to be elucidated yet. To improve knowledge on the effects played by microplastics on free-living and fish gut-associated microbial community in aquatic environments, a 90-day study was performed in three replicated mesocosms (control-CTRL, native polyvinyl chloride-MPV and weathered polyvinyl chloride-MPI), where sea bass specimens were hosted. In CTRL mesocosm, fish was fed with no-plastic-added food, whilst in MPV and MPI food was supplemented with native or exposed to polluted waters polyvinylchloride pellets, respectively. Particulate organic carbon (POC) and nitrogen, total and culturable bacteria, extracellular enzymatic activities, and microbial community substrate utilization profiles were analyzed. POC values were lower in MPI than MPV and CRTL mesocosms. Microplastics did not affect severely bacterial metabolism, although enzymatic activities decreased and microbes utilized a lower number of carbon substrates in MPI than MPV and CTRL. No shifts in the bacterial community composition of fish gut microflora were observed by denaturing gradient gel electrophoresis fingerprinting analysis.

Keywords

Microplastics Microbial community Metabolism Fish gut microbiota Mesocosm 

Abbreviations

CTRL

Control water tank

MPV

water tank added with native polyvinyl chloride

MPI

water tank added with weathered polyvinyl chloride

Notes

Acknowledgements

The authors are grateful to technician personnel of the CNR-IAMC Aquaculture Experimental Facilities of Messina. In particular, they thank Sig. Antonino Parisi, who provided his support in technical execution of experiment.

Supplementary material

11356_2018_2926_MOESM1_ESM.doc (86 kb)
Fig. S1 Mean values ± standard deviation of Biochemical Oxygen Demand (BOD5) measured over time in the control (CTRL, white circles), virgin microplastics (MPV, grey circles) and weathered microplastics (MPI, black circles) treated tanks. Asterisks indicate significant differences related to the variable “treatment”, whilst different letters indicate significant differences related to the variable “time. n = 3 replicated measurements. (DOC 86 kb)
11356_2018_2926_MOESM2_ESM.docx (2 mb)
Fig. S2 Denaturing Gradient Gel Electrophoresis (DGGE) banding profiles obtained by fingerprinting analysis of the 16S rDNA of gut bacterial communities of fish kept in the control (CTRL, white circles), virgin microplastics (MPV, grey circles) and weathered microplastics (MPI, black circles) treated tanks. The arrows show the excised bands. L, ladder. (DOCX 2060 kb)
11356_2018_2926_MOESM3_ESM.doc (82 kb)
Fig. S3 (A, B) Outputs of Cluster analysis (A) and non-metric MultiDimensional Scaling (n-MDS) analysis (B) performed on gut microbiota of fish kept in the control (CTRL), virgin microplastics (MPV) and weathered microplastics (MPI) treated tanks after 30, 60 and 90 days. (DOC 82 kb)
11356_2018_2926_MOESM4_ESM.doc (56 kb)
Table S1 Mean values ± standard deviation of the main physical-chemical values of seawater measured per each treatment (CTRL: Control; MPV: native, virgin microplastics; MPI: weathered microplastics) and per each sampling time (where T0 and T90 are the start and the end of the experiment). n = 3 replicated measurements. (DOC 55 kb)
11356_2018_2926_MOESM5_ESM.docx (47 kb)
Table S2 Raw substrate utilization obtained on Biolog Eco-plates, reported as Averaged Substrate Colour Development (ASCD) per each treatment (Control, CTRL; Virgin Microplastics, MPV and Weathered Microplastics, MPI) over time (T0, T30, T60 and T90 where T0 is the start and T90 is the end of the experiment) and number of substrates (n) with a positive response having OD > 0.10. D = days of experiment. (DOCX 46 kb)
11356_2018_2926_MOESM6_ESM.docx (39 kb)
Table S3 Diversity indices obtained by Averaged Substrate Colour Development (ASCD) ± standard deviation on Biolog Eco-plates, per each time (T0, T30, T60 and T90 where T0 is the start and T90 is the end of the experiment) and treatment (Control, CTRL; Virgin Microplastics, MPV and Weathered Microplastics, MPI). Mean value of positive wells over each experiment time (n), substrate richness (S), Shannon functional diversity index (H′), Pielou’s Evenness index (E) and average proportion of ASCD per substrate (ASCD/S). (DOCX 38 kb)
11356_2018_2926_MOESM7_ESM.docx (15 kb)
Table S4 16S rDNA gene sequence affiliation of the excised DGGE bands to their closest phylogenetic neighbors (CTRL: Control; MPV: native, virgin microplastics; MPI: weathered microplastics). (DOCX 14 kb)

References

  1. Amaral-Zettler LA, Zettler ER, Slikas B, Boyd GD, Melvin DW, Morrall CE, Proskurowski G, Mincer TJ (2015) The biogeography of the plastisphere: implications for policy. Front Ecol Environ 13:541–546.  https://doi.org/10.1890/150017 CrossRefGoogle Scholar
  2. Andersson E (2014) Microplastics in the oceans and their effect on the marine fauna. Sveriges lantbruksuniversitet. Fakulteten för veterinärmedicin och husdjursvetenskap, pp. 1-14Google Scholar
  3. Andrady AL (2011) Microplastics in the marine environment. Mar Pollut Bull 62:1596–1605.  https://doi.org/10.1016/j.marpolbul.2011.05.030 CrossRefGoogle Scholar
  4. Avio CG, Gorbi S, Regoli F (2017) Plastics and microplastics in the oceans: from emerging pollutants to emerged threat. Mar Environ Res 128:2–11.  https://doi.org/10.1016/j.marenvres.2016.05.012 CrossRefGoogle Scholar
  5. Battaglia P, Pedà C, Musolino S, Esposito V, Andaloro F, Romeo T (2015) Diet and first documented data on plastic ingestion of Trachinotus ovatus L. 1758 (Pisces: Carangidae) from the Strait of Messina (Central Mediterranean Sea). Ital J Zool 1-9, DOI:  https://doi.org/10.1080/11250003.2015.1114157 CrossRefGoogle Scholar
  6. Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson RC (2008) Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.). Environ Sci Technol 42:5026–5031.  https://doi.org/10.1021/es800249a CrossRefGoogle Scholar
  7. Bryant JA, Clemente TM, Viviani DA, Fong AA, Thomas KA, Kemp P, Karl DM, White AE, DeLong EF (2016) Diversity and activity of communities inhabiting plastic debris in the North Pacific gyre. MSystems 1:e00024–e00016.  https://doi.org/10.1128/mSystems.00024-16 CrossRefGoogle Scholar
  8. Cappello S, Caruso G, Zampino D, Monticelli LS, Maimone G, Denaro R, Tripodo B, Troussellier M, Yakimov M, Giuliano L (2007) Microbial community dynamics during assays of harbour oil spill bioremediation: a microscale simulation study. J Appl Microbiol 102(1):184–194.  https://doi.org/10.1111/j.1365-2672.2006.03071.x CrossRefGoogle Scholar
  9. Carda-Diéguez M, Mira A, Fouz B (2014) Pyrosequencing survey of intestinal microbiota diversity in cultured sea bass (Dicentrarchus labrax) fed functional diets. FEMS Microbiol Ecol 87:451–459.  https://doi.org/10.1111/1574-6941.12236 CrossRefGoogle Scholar
  10. Carson HS, Nerheim MS, Carroll KA, Eriksen M (2013) The plastic-associated microorganisms of the North Pacific gyre. Mar Pollut Bull 75:126–132.  https://doi.org/10.1016/j.marpolbul.2013.07.054 CrossRefGoogle Scholar
  11. Caruso G (2010) Leucine aminopeptidase, beta-glucosidase and alkaline phosphatase activity rates and their significance in carbon and phosphorus cycles in some coastal Mediterranean sites. Mar Drugs 8(4):916–940.  https://doi.org/10.3390/md8040916 CrossRefGoogle Scholar
  12. Caruso G (2015) Microplastics in marine environments: possible interactions with the microbial assemblage. J Pollut Eff Controls 3:e111.  https://doi.org/10.4172/2375-4397.1000e111 CrossRefGoogle Scholar
  13. Caruso G, Genovese L, Mancuso M, Modica A (2003) Effects of fish farming on microbial enzyme activities and densities: comparison between three Mediterranean sites. Lett Appl Microbiol 37:324–328.  https://doi.org/10.1046/j.1472-765X.2003.01401.x CrossRefGoogle Scholar
  14. Caruso G, La Ferla R, Azzaro M, Zoppini A, Marino G, Petochi T, Corinaldesi C, Leonardi M, Zaccone R, Fonda Umani S, Caroppo C, Monticelli LS, Azzaro F, Decembrini F, Maimone G, Cavallo RA, Stabili L, Todorova NH, Karamfilov VK, Rastelli E, Cappello S, Acquaviva MI, Narracci M, De Angelis R, Del Negro P, Latini M, Danovaro R (2016) Microbial assemblages for environmental quality assessment: knowledge, gaps and usefulness in the European marine strategy framework directive. Crit Rev Microbiol 42(6):883–904.  https://doi.org/10.3109/1040841X.2015.1087380 CrossRefGoogle Scholar
  15. Christian BW, Lind OT (2006) Key issues concerning biolog use for aerobic and anaerobic freshwater bacterial community-level physiological profiling. Int Rev Hydrobiol 91(3):257–268.  https://doi.org/10.1002/iroh.200510838 CrossRefGoogle Scholar
  16. Clarke KR, Gorley RN (2005) PRIMER: getting started with v6. PRIMER-E Ltd, Plymouth Marine Laboratory, Plymouth, UKGoogle Scholar
  17. Cole M, Lindeque P, Halsband C, Galloway TS (2011) Microplastics as contaminants in the marine environment: a review. Mar Pollut Bull 62:2588–2597.  https://doi.org/10.1016/j.marpolbul.2011.09.025 CrossRefGoogle Scholar
  18. Cole M, Lindeque P, Fileman E, Halsband C, Goodhead R, Moger J, Galloway TS (2013) Microplastic ingestion by zooplankton. Environ Sci Technol 47:6646–6655.  https://doi.org/10.1021/es400663f CrossRefGoogle Scholar
  19. De Schryver P, Dierckens K, Thi QQ, Amalia R, Marzorati M, Bossier P, Boon N, Verstraete W (2011) Convergent dynamics of the juvenile European sea bass gut microbiota induced by poly-beta-hydroxybutyrate. Environ Microbiol 13:1042–1051.  https://doi.org/10.1111/j.1462-2920.2010.02410.x CrossRefGoogle Scholar
  20. De Tender CA, Devriese LI, Haegeman A, Maes S, Ruttink T, Dawyndt P (2015) Bacterial community profiling of plastic litter in the Belgian part of the North Sea. Environ Sci Technol 49:9629–9638.  https://doi.org/10.1021/acs.est.5b01093 CrossRefGoogle Scholar
  21. Deudero S, Alomar C (2015) Mediterranean marine biodiversity under threat: reviewing influence of marine litter on species. Mar Pollut Bull 98(1):58–68.  https://doi.org/10.1016/j.marpolbul.2015.07.012 CrossRefGoogle Scholar
  22. Eerkes-Medrano D, Thompson RC, Aldridge DC (2015) Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Res 75:63–82.  https://doi.org/10.1016/j.watres.2015.02.012 CrossRefGoogle Scholar
  23. Espinosa C, Cuesta A, Esteban MA (2017) Effects of dietary polyvinylchloride microparticles on general health, immune status and expression of several genes related to stress in gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 68:251–259.  https://doi.org/10.1016/j.fsi.2017.07.006 CrossRefGoogle Scholar
  24. European Commission (2008) Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). In Official Journal of the European Union, 25 June 2008, L 164, pp. 19–40Google Scholar
  25. Farrell P, Nelson K (2013) Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environ Pollut 177:1–3.  https://doi.org/10.1016/j.envpol.2013.01.046 CrossRefGoogle Scholar
  26. Fortuño J, Masó M, Sáez R, De Juan S, Demestre M (2010) SEM microphotographs of biofouling organisms on floating and benthic plastic debris. Rapp Comm Int Explor sci Mer Medit 39:358Google Scholar
  27. Fossi MC, Coppola D, Baini M, Giannetti M, Guerranti C, Marsili L, Panti C, De Sabata E, Clò S (2014) Large filter feeding marine organisms as indicators of microplastic in the pelagic environment: the case studies of the Mediterranean basking shark (Cetorhinus maximus) and fin whale (Balaenoptera physalus). Mar Environ Res 100:17–24.  https://doi.org/10.1016/j.marenvres.2014.02.002 CrossRefGoogle Scholar
  28. Fossi MC, Panti C, Guerranti C, Coppola D, Giannetti M, Marsili L, Minutoli R (2012) Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Mar Pollut Bull 64(11):2374–2379.  https://doi.org/10.1016/j.marpolbul.2012.08.013 CrossRefGoogle Scholar
  29. Galgani F, Fleet D, Van Franeker J, Katsanevakis S, Maes T, Mouat J, Oosterbaan L, Poitou I, Hanke G, Thompson R, Amato E, Birkun A, Janssen C (2010) Marine strategy framework directive – task group 10 report marine litter, joint report. In: Zampoukas N (ed) Joint Research Centre Scientific and Technical Reports. Office for Official Publications of the European Communities, Luxembourg, EUR 24340, pp. 1–57. ENDOI:  https://doi.org/10.2788/86941
  30. Galgani F, Barnes DKA, Deudero S, Fossi MC, Ghiglione JF, Hema T, Jorissen FJ, Karapanagioti HK, Katsanevakis S, Klasmeier J, von Moos N, Pedrotti ML, Raddadi N, Sobral P, Zambianchi E, Briand F (2014) Executive summary. In: Briand F (ed) Marine litter in the Mediterranean and Black Seas. CIESM Workshop Monograph 46. CIESM Publisher, Monaco, pp 7–20Google Scholar
  31. Galloway TS, Cole M, Lewis C (2017) Interactions of microplastic debris throughout the marine ecosystem. Nat Ecol Evol 1:0116.  https://doi.org/10.1038/s41559-017-0116 CrossRefGoogle Scholar
  32. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359Google Scholar
  33. Gavrilescu M (2010) Dynamic biochemistry. Proc Biotechnol Mol Biol 4:1–36Google Scholar
  34. Genovese M, Crisafi F, Denaro R, Cappello S, Russo D, Calogero R, Santisi S, Catalfamo M, Modica A, Smedile F, Genovese L, Golyshin PN, Giuliano L, Yakimov M (2014) Effective bioremediation strategy for rapid in situ cleanup of anoxic marine sediments in mesocosm oil spill simulation. Front Microbiol 5:162.  https://doi.org/10.3389/fmicb.2014.00162 CrossRefGoogle Scholar
  35. Grigorakis S, Mason SA, Drouillard KG (2017) Determination of the gut retention of plastic microbeads and microfibers in goldfish (Carassius auratus). Chemosphere 169:233–238.  https://doi.org/10.1016/j.chemosphere.2016.11.055 CrossRefGoogle Scholar
  36. Güven O, Gökdağ K, Jovanović B, Kıdeyş AE (2017) Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ Pollut 223:286–294.  https://doi.org/10.1016/j.envpol.2017.01.025 CrossRefGoogle Scholar
  37. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4(1):1–9 Available at http://palaeo-electronica.org/2001_1/past/issue1_01.htm Google Scholar
  38. Harrison JP, Sapp M, Schratzberger M, Osborn AM (2011) Interactions between microorganisms and marine microplastics: a call for research. Mar Technol Soc J 45:12–20.  https://doi.org/10.4031/MTSJ.45.2.2 CrossRefGoogle Scholar
  39. Harrison JP, Schratzberger M, Sapp M, Osborn AM (2014) Rapid bacterial colonization of low-density polyethylene microplastics in coastal sediment microcosms. BMC Microbiol 14:232.  https://doi.org/10.1186/s12866-014-0232-4 CrossRefGoogle Scholar
  40. Hoellein T, Rojas M, Pink A, Gasior J, Kelly J (2014) Anthropogenic litter in urban freshwater ecosystems: distribution and microbial interactions. PLoS One 9:e98485.  https://doi.org/10.1371/journal.pone.0098485 CrossRefGoogle Scholar
  41. Hoppe HG, Arnosti C, Herndl GJ (2002) Ecological significance of bacterial enzymes in the marine environment. In: Burns R, Dick R (eds) Enzymes in the environment: activity. Ecology and Applications. Marcel Dekker, New York, pp 73–108.  https://doi.org/10.1201/9780203904039.ch3 CrossRefGoogle Scholar
  42. Iseki K, MacDonald RW, Carmack E (1987) Distribution of particulate matter in the south-eastern Beaufort Sea in late summer. Proceedings NIPR Symposium Polar Biol 1:35–46Google Scholar
  43. Jałowiecki Ł, Chojniak JM, Dorgeloh E, Hegedusova B, Ejhed H, Magnér J, Plaza GA (2016) Microbial community profiles in wastewaters from onsite wastewater treatment systems technology. PLoS One 11(1):e0147725.  https://doi.org/10.1371/journal.pone.0147725 CrossRefGoogle Scholar
  44. Jovanovic B (2017) Ingestion of microplastics by fish and its potential consequences from a physical perspective. Integr Environ Assess Manag 13(3):510–515.  https://doi.org/10.1002/ieam.1913 CrossRefGoogle Scholar
  45. Keswani A, Oliver DM, Gutierrez T, Quilliam RS (2016) Microbial hitchhikers on marine plastic debris: human exposure risks at bathing waters and beach environments. Mar Environ Res 118:10–19.  https://doi.org/10.1016/j.marenvres.2016.04.006 CrossRefGoogle Scholar
  46. Kirstein IV, Kirmizi S, Wichels A, Garin-Fernandez A, Erler R, Löder M, Gerdts G (2016) Dangerous hitchhikers? Evidence for potentially pathogenic Vibrio spp. on microplastic particles. Mar Environ Res 120:1–8.  https://doi.org/10.1016/j.marenvres.2016.07.004 CrossRefGoogle Scholar
  47. Kurten GL and Barkoh A (2014) Evaluation of community-level physiological profiling for monitoring microbial community function in fish hatchery ponds. Texas Parks and Wildlife Department Inland Fisheries Division, management data series no. 279. Austin, Texas 78744Google Scholar
  48. La Ferla R, Azzaro M, Michaud L, Caruso G, Lo Giudice A, Paranhos R, Cabral AS, Conte A, Cosenza A, Maimone G, Papale M, Rappazzo AC, Guglielmin M (2017) Prokaryotic abundance and activity in permafrost of the northern Victoria land and upper Victoria Valley (Antarctica). Microb Ecol 74(2):402–415.  https://doi.org/10.1007/s00248-017-0955-5 CrossRefGoogle Scholar
  49. Lenz R, Enders K, Gissel Nielsen TG (2016) Microplastic exposure studies should be environmentally realistic. PNAS 113:E4121–E4122.  https://doi.org/10.1073/pnas.1606615113 CrossRefGoogle Scholar
  50. Lobelle D, Cunliffe M (2011) Early microbial biofilm formation on marine plastic debris. Mar Pollut Bull 62:197–200.  https://doi.org/10.1016/j.marpolbul.2010.10.013 CrossRefGoogle Scholar
  51. Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol 10:1571–1581.  https://doi.org/10.1111/j.1462-2920.2008.01572.x CrossRefGoogle Scholar
  52. Mattsson K, Ekvall MT, Hansson L-A, Linse S, Malmendal A, Cedervall T (2015) Altered behavior, physiology, and metabolism in fish exposed to polystyrene nanoparticles. Environ Sci Technol 49:553–561.  https://doi.org/10.1021/es5053655 CrossRefGoogle Scholar
  53. Mazurais D, Ernande B, Quazuguel P, Severe A, Huelvan C, Madec L, Mouchel O, Soudant P, Robbens J, Huvet A, Zambonino-Infante J (2015) Evaluation of the impact of polyethylene microbeads ingestion in European sea bass (Dicentrarchus labrax) larvae. Mar Environ Res 112:78–85.  https://doi.org/10.1016/j.marevres.2015.09.009 CrossRefGoogle Scholar
  54. McCormick A, Hoellein TJ, Mason SA, Schluep J, Kelly JJ (2014) Microplastic is an abundant and distinct microbial habitat in an urban river. Environ Sci Technol 48(20):11863–11871.  https://doi.org/10.1021/es503610r CrossRefGoogle Scholar
  55. Merrifield DL, Harper GM, Mustafa S, Carnevali O, Picchietti S, Davies SJ (2011) Effect of dietary alginic acid on juvenile tilapia (Oreochromis niloticus) intestinal microbial balance, intestinal histology and growth performance. Cell Tissue Res 344:135–146.  https://doi.org/10.1007/s00441-010-1125-y CrossRefGoogle Scholar
  56. Michaud L, Di Marco G, Bruni V, Lo Giudice A (2007) Biodegradative potential and characterization of psychrotolerant polychlorinated biphenyl-degrading bacteria isolated from a coastal station in Terra Nova Bay (Ross Sea, Antarctica). Mar Pollut Bull 54:1754–1761.  https://doi.org/10.1016/j.marpolbul.2007.07.011 CrossRefGoogle Scholar
  57. Moosavi M (2017) Bentonite clay as a natural remedy: a brief review. Iran J Public Health 46(9):1176–1183Google Scholar
  58. NOAA (National Oceanic and Atmospheric Administration) (2014) http://www.deq.state.va.us/programs/coastalzonemanagment.aspx.
  59. Oberbeckmann S, Löder MG, Gerdts G, Osborn AM (2014) Spatial and seasonal variation in diversity and structure of microbial biofilms on marine plastics in northern European waters. FEMS Microbiol Ecol 90:478–492.  https://doi.org/10.1111/1574-6941.12409 CrossRefGoogle Scholar
  60. Oberbeckmann S, Löder MGJ, Labrenz M (2015) Marine microplastic-associated biofilms—a review. Environ Chem 12:551–562.  https://doi.org/10.1071/en15069 CrossRefGoogle Scholar
  61. Pedà C, Caccamo L, Fossi MC, Gai F, Andaloro F, Genovese L, Perdichizzi A, Romeo T, Maricchiolo G (2016) Intestinal alterations in European sea bass Dicentrarchus labrax (Linnaeus, 1758) exposed to microplastics: preliminary results. Environ Pollut 212:251–256.  https://doi.org/10.1016/j.envpol.2016.01.083 CrossRefGoogle Scholar
  62. Pedà C, Maricchiolo G, Caccamo L, Perdichizzi A, Gai F, Consoli P, Esposito V, Fossi MC, Andaloro F, Genovese L, Romeo T (2017) Histological evidences for mechanical and physical damages induced by microplastics in the intestine of European sea bass, Dicentrarchus labrax (Linnaeus, 1758). SETAC Europe 27th Annual Meeting Abstract Book p. 330Google Scholar
  63. Pérez-Rodríguez M, Cortizas AM (2014) Preliminary characterization of microbial functional diversity using sole-C-source utilization profiles in Tremoal do Pedrido mire (Galicia, NW Spain). Spanish J Soil Sci 4(2):158–178.  https://doi.org/10.3232/SJSS.2014.V4.N2.03 CrossRefGoogle Scholar
  64. Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles: a critique. FEMS Microbiol Ecol 42:1–14.  https://doi.org/10.1111/j.1574-6941.2002.tb00990.x CrossRefGoogle Scholar
  65. Quilliam RS, Jamieson J, Oliver DM (2014) Seaweeds and plastic debris can influence the survival of faecal indicator organisms in beach environments. Mar Pollut Bull 84:201–207.  https://doi.org/10.1016/j.marpolbul.2014.05.011 CrossRefGoogle Scholar
  66. Reisser J, Shaw J, Hallegraeff G, Proietti M, Barnes DKA, Thums M, Wilcox C, Hardesty BD, Pattiaratchi C (2014) Millimeter-sized marine plastics: a new pelagic habitat for microorganisms and invertebrates. PLoS One 9:e100289.  https://doi.org/10.1371/journal.pone.0100289 CrossRefGoogle Scholar
  67. Rios LM, Moore C, Jones PR (2007) Persistent organic pollutants carried by synthetic polymers in the ocean environment. Mar Poll Bull 54:1230–1237.  https://doi.org/10.1016/j.marpolbul.2007.03.022 CrossRefGoogle Scholar
  68. Rochman CM, Hoh E, Hentschel BT, Kaye S (2013) Long-term field measurements of sorption of organic contaminants to five types of plastic pellets: implications for plastic marine debris. Environ Sci Technol 47:1646–1654.  https://doi.org/10.1021/es303700s CrossRefGoogle Scholar
  69. Romeo T (2011) Monitoraggio ambientale dell'area di Milazzo attraverso l’utilizzo di biondicatori al fine di una valutazione della biodiversità e dell’ecosistema marino. Relazione finale, pp:1–148Google Scholar
  70. Romeo T, Pietro B, Pedà C, Consoli P, Andaloro F, Fossi MC (2015) First evidence of presence of plastic debris in stomach of large pelagic fish in the Mediterranean Sea. Mar Pollut Bull 95(1):358–361.  https://doi.org/10.1016/j.marpolbul.2015.04.048 CrossRefGoogle Scholar
  71. Romeo T, Pedà C, Fossi MC, Andaloro F, Battaglia P (2016) First record of plastic debris in the stomach of Mediterranean lantern fishes. Acta Adriat 56(2):145–156Google Scholar
  72. Rummel CD, Löder MGJ, Fricke NF, Lang T, Griebeler E-M, Janke M, Gerdts G (2016) Plastic ingestion by pelagic and demersal fish from the North Sea and Baltic Sea. Mar Pollut Bull 102:134–141.  https://doi.org/10.1016/j.marpolbul.2015.11.043 CrossRefGoogle Scholar
  73. Rutgers M, Wouterse M, Drost SM, Breure AM, Mulder C, Stone D, Creamer RE, Winding A, Bloem J (2016) Monitoring soil bacteria with community-level physiological profiles using biolog™ ECO-plates in the Netherlands and Europe. Appl Soil Ecol 97:23–35.  https://doi.org/10.1016/j.apsoil.2015.06.007 CrossRefGoogle Scholar
  74. Sala MM, Arin L, Balagué V, Felipe J, Guadayol O, Vaqué D (2005) Functional diversity of bacterioplankton assemblages in western Antarctic seawaters during late spring. Mar Ecol Progr Ser 292:13–21.  https://doi.org/10.3354/meps292013 CrossRefGoogle Scholar
  75. Sala MM, Estrada M, Gasol JM (2006) Seasonal changes in the functional diversity of bacterioplankton in contrasting coastal environments of the NW Mediterranean. Aquat Microb Ecol 44:1–9.  https://doi.org/10.3354/ame044001 CrossRefGoogle Scholar
  76. Suaria G, Avio CG, Mineo A, Lattin GL, Magaldi MG, Belmonte G, Moore CJ, Regoli F, Aliani S (2016) The Mediterranean plastic soup: synthetic polymers in Mediterranean surface waters. Sci Rep 6:37551.  https://doi.org/10.1038/srep37551 CrossRefGoogle Scholar
  77. Teuten EL, Saquing JM, Knappe DRU, Balaz MA, Jonsson S, Bjorn A, Roland SJ, Thompson RC, Galloway TS, Yamashita R, Ochi D, Watanuki Y, Moore C, Pham HV, Tana TS, Prudente M, Boonyatumanond R, Zakaria MP, Akkhavong K, Ogata Y, Hirai H, Iwasa S, Mizukawa K, Hagino Y, Imamura A, Saha M, Takada H (2009) Transport and release of chemicals from plastics to the environment and to wildlife. Philos Trans R Soc B Biol Sci 364(1526):2027–2045.  https://doi.org/10.1098/rstb.2008.0284 CrossRefGoogle Scholar
  78. Thompson RC, Olsen Y, Mitchell RP, Davis A, Rowland SJ, John AW, McGonigle D, Russell AE (2004) Lost at sea: where is all the plastic? Science 304(5672):838.  https://doi.org/10.1126/science.1094559 CrossRefGoogle Scholar
  79. UNEP (United Nations Environment Programme) (2005) Marine litter. An analytical overview, pp 1–58Google Scholar
  80. US EPA (United States Environmental Protection Agency) (1992) 2C. Final Report. EPA842-B-92-010Google Scholar
  81. Wagner M, Scherer C, Alvarez-Muñoz D, Brennholt N, Bourrain X, Buchinger S, Fries E, Grosbois C, Klasmeier J, Marti T, Rodriguez-Mozaz S, Urbatzka R, Vethaak AD, Winther-Nielsen M, Reifferscheid G (2014) Microplastics in freshwater ecosystems: what we know and what we need to know. Environ Sci Eur 26:12.  https://doi.org/10.1186/s12302-014-0012-7 CrossRefGoogle Scholar
  82. Wang J, Tan Z, Peng J, Qiu Q, Li M (2016) The behaviors of microplastics in the marine environment. Mar Environ Res 113:7–17.  https://doi.org/10.1016/j.marenvres.2015.10.014 CrossRefGoogle Scholar
  83. Yakimov M, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, Timmis KN, Golyshin PN, Giuliano L (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7(9):1426–1441.  https://doi.org/10.1111/j.1462-5822.2005.00829.x CrossRefGoogle Scholar
  84. Yang H-L, Sun Y-Z, Ma R-L, Ye J-D (2012) PCR-DGGE analysis of the autochthonous gut microbiota of grouper Epinephelus coioides following probiotic Bacillus clausii administration. Aquac Res 43:489–497.  https://doi.org/10.1111/j.1365-2109.2011.02852.x CrossRefGoogle Scholar
  85. Zettler ER, Mincer TJ, Amaral-Zettler LA (2013) Life in the “plastisphere”: microbial communities on plastic marine debris. Environ Sci Technol 47:7137–7146.  https://doi.org/10.1021/es401288x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Gabriella Caruso
    • 1
  • Cristina Pedà
    • 2
  • Simone Cappello
    • 1
  • Marcella Leonardi
    • 1
  • Rosabruna La Ferla
    • 1
  • Angelina Lo Giudice
    • 1
    • 3
  • Giulia Maricchiolo
    • 1
  • Carmen Rizzo
    • 3
  • Giovanna Maimone
    • 1
  • Alessandro Ciro Rappazzo
    • 1
  • Lucrezia Genovese
    • 1
  • Teresa Romeo
    • 2
  1. 1.National Research Council, Institute for Coastal Marine Environment (CNR-IAMC)MessinaItaly
  2. 2.Institute for Environmental Protection and Research (ISPRA)MilazzoItaly
  3. 3.Department of Chemical, Biological, Pharmaceutical and Environmental SciencesUniversity of MessinaMessinaItaly

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