Fouling Microbial Communities on Plastics Compared with Wood and Steel: Are They Substrate- or Location-Specific?
Although marine biofouling has been widely studied on different substrates, information on biofouling on plastics in the Arabian Gulf is limited. Substrate- and location-specific effects were investigated by comparing the microbial communities developed on polyethylene terephthalate (PET) and polyethylene (PE) with those on steel and wood, at two locations in the Sea of Oman. Total biomass was lower on PET and PE than on steel and wood. PET had the highest bacterial abundance at both locations, whereas chlorophyll a concentrations did not vary between substrates. MiSeq 16S ribosomal RNA sequencing revealed comparable operational taxonomic unit (OTU) richness on all substrates at one location but lower numbers on PET and PE at the other location. Non-metric multidimensional scaling (NMDS) showed distinct clusters of the bacterial communities based on substrate (analysis of similarity (ANOSIM), R = 0.45–0.97, p < 0.03) and location (ANOSIM, R = 0.56, p < 0.0001). The bacterial genera Microcystis and Hydrogenophaga and the diatoms Licmophora and Mastogloia were specifically detected on plastics. Desulfovibrio and Pseudomonas spp. exhibited their highest abundance on steel and Corynebacterium spp. on wood. Scanning electron microscopy (SEM) revealed fissure formation on PET and PE, indicating physical degradation. The presence of free radicals on PET and carbonyl bonds (C=O) on PE, as revealed by Fourier transform infrared (FTIR) spectroscopy, indicated abiotic degradation while hydroxyl groups and spectral peaks for proteins and polysaccharides on PE indicated biotic degradation. We conclude that fouling microbial communities are not only substrate-specific but also location-specific and microbes developing on plastics could potentially contribute to their degradation in the marine environment.
KeywordsBiofouling Substrates Plastic MiSeq FTIR SEM
We would like to thank Mr. Ahmed Al Rawahi and Mr. Abdullah Al Nashri for their help during the experimental setup and sample collection. We would also like to acknowledge the Technical Unit of University of Nizwa and Dr. Abdul Munam, Sultan Qaboos University, for their kind guidance during the FTIR analysis and data interpretation. RA would like to thank the Hanse-Wissenschaftskolleg (HWK), Institute for Advanced Study, Germany, for supporting his study group.
This research was financially supported by the collaborative grant (SQU-GCC/CL/17/02).
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- 2.Eriksen M, Lebreton LC, Carson HS, Thiel M, Moore CJ, Borerro JC, Galgani F, Ryan PG, Reisser J (2014) Plastic pollution in the world’s oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS One 9:e111913. https://doi.org/10.1371/journal.pone.0111913 CrossRefPubMedPubMedCentralGoogle Scholar
- 12.Pierce KE, Harris RJ, Larned LS, Pokras MA (2004) Obstruction and starvation associated with plastic ingestion in a northern gannet Morus bassanus and a greater shearwater Puffinus gravis. Mar Ornithol 32:187–189Google Scholar
- 16.Lusher AL, Hernandez-Milian G, O’Brien J, Berrow S, O’Connor I, Officer R (2015a) Microplastic and macroplastic ingestion by a deep diving, oceanic cetacean: the True’s beaked whale Mesoplodon mirus. Environ Pollut 199:185–191. https://doi.org/10.1016/j.envpol.2015.01.023 CrossRefPubMedGoogle Scholar
- 22.Eich A, Mildenberger T, Laforsch C, Weber M (2015) Biofilm and diatom succession on polyethylene (PE) and biodegradable plastic bags in two marine habitats: early signs of degradation in the pelagic and benthic zone? PLoS One 10:e0137201. https://doi.org/10.1371/journal.pone.0137201 CrossRefPubMedPubMedCentralGoogle Scholar
- 32.Sudhakar M, Trishul A, Doble M, Kumar KS, Jahan SS, Inbakandan D, Viduthalai RR, Umadevi VR, Murthy PS, Venkatesan R (2007) Biofouling and biodegradation of polyolefins in ocean waters. Polym Degrad Stab 92:1743–1752. https://doi.org/10.1016/j.polymdegradstab.2007.03.029 CrossRefGoogle Scholar
- 34.Dussud C, Hudec C, George M, Fabre P, Higgs P, Bruzaud S, Delort AM, Eyheraguibel B, Meistertzheim AL, Jacquin J, Cheng J, Callac N, Odobel C, Rabouille S, Ghiglione JF (2018) Colonization of nonbiodegradable and biodegradable plastics by marine microorganisms. Front Microbiol 9:1571Google Scholar
- 35.Harshvardhan K, Jha B (2013) Biodegradation of low-density polyethylene by marine bacteria from pelagic waters, Arabian Sea, India. Marine Poll Bull 77:100–106Google Scholar
- 40.Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. https://doi.org/10.1093/nar/gks808 CrossRefPubMedPubMedCentralGoogle Scholar
- 42.Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
- 43.Abed RMM, Al Kindi S, Schramm A, Barry MJ (2011) Short-term effects of flooding on bacterial community structure and nitrogenase activity in microbial mats from a desert stream. Aquat Microb Ecol 63:245–254Google Scholar
- 45.Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software: package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
- 48.Dang H, Lovell CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66:467–475. https://doi.org/10.1128/AEM.66.2.467-475.2000 CrossRefPubMedPubMedCentralGoogle Scholar
- 53.Kumar NV, Venkatesan R, Doble M (2014) Macrofouling and bioadhesion of organisms on polymers. In: Doble R, Venkatesan R, Kumar NV (eds) Polymers in a marine environment. Smithers RapraTechnology, p 101–120Google Scholar
- 56.Wen G, Kötzsch S, Vital M, Egli T, Ma J (2015) BioMig-A method to evaluate the potential release of compounds from and the formation of biofilms on polymeric materials in contact with drinking water. Environ Sci Technol 49:11659–11669. https://doi.org/10.1021/acs.est.5b02539 CrossRefPubMedPubMedCentralGoogle Scholar
- 57.Fries E, Dekiff JH, Willmeyer J, Nuelle MT, Ebert M, Remy D (2013) Identification of polymer types and additives in marine microplastic particles using pyrolysis-GC/MS and scanning electron microscopy. Environ Sci Process Impacts 15:1949–1956. https://doi.org/10.1039/C3EM00214D CrossRefPubMedPubMedCentralGoogle Scholar
- 60.Reynolds CS (1997) Vegetation processes in the pelagic: a model for ecosystem theory Oldendorf/Luhe: Ecology InstituteGoogle Scholar
- 68.Witt V, Wild C, Anthony K, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the great barrier reef. Environ Microbiol 13:2976–2989. https://doi.org/10.1111/j.1462-2920.2011.02571.x CrossRefPubMedPubMedCentralGoogle Scholar
- 69.Lidbury I, Johnson V, Hall-Spencer JM, Munn CB, Cunliffe M (2012) Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem. Mar Pollut Bull 64:1063–1066. https://doi.org/10.1016/j.marpolbul.2012.02.011 CrossRefPubMedPubMedCentralGoogle Scholar
- 75.Brinkhoff T, Bach G, Heidorn T, Liang L, Schlingloff A, Simon M (2004) Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates. Appl Environ Microbiol 70:2560–2565. https://doi.org/10.1128/AEM.70.4.2560-2565.2003 CrossRefPubMedPubMedCentralGoogle Scholar
- 76.Greer EM, Aebisher D, Greer A, Bentley R (2008) Computational studies of the Tropone natural products, Thiotropocin, Tropodithietic acid, and Troposulfenin. Significance of Thiocarbonyl–enol Tautomerism. J Org Chem 73:280–283. https://doi.org/10.1021/jo7018416 CrossRefPubMedPubMedCentralGoogle Scholar
- 77.D’Alvise PW, Phippen CB, Nielsen KF, Gram L (2016) Influence of iron on production of the antibacterial compound tropodithietic acid and its noninhibitory analog in Phaeobacter inhibens. Appl Environ Microbiol 82:502–509. https://doi.org/10.1128/AEM.02992-15 CrossRefPubMedPubMedCentralGoogle Scholar
- 89.Reisser J, Shaw J, Hallegraeff G, Proietti M, Barnes DK, 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 96.Venkatachalam SG, Nayak SG, Labde JV, Gharal PR, Rao K, Kelkar AK (2012) Degradation and recyclability of poly (ethylene terephthalate). In: Polyester, InTech, pp 75–98Google Scholar
- 97.Fotopoulou KN, Karapanagioti HK (2017) Degradation of various plastics in the environment. The handbook of environmental chemistry. Springer, Berlin, pp 1–22Google Scholar
- 99.Linos A, Berekaa MM, Reichelt R, Keller U, Schmitt J, Flemming HC, Kroppenstedt RM, Steinbüchel A (2000) Biodegradation of cis-1, 4-polyisoprene rubbers by distinct actinomycetes: microbial strategies and detailed surface analysis. Appl Environ Microbiol 66:1639–1645. https://doi.org/10.1128/AEM.66.4.1639-1645.2000 CrossRefPubMedPubMedCentralGoogle Scholar
- 101.Balasubramanian V, Natarajan K, Hemambika B, Ramesh N, Sumathi CS, Kottaimuthu R, Rajesh Kannan V (2010) High-density polyethylene (HDPE)-degrading potential bacteria from marine ecosystem of Gulf of Mannar, India. Lett Appl Microbiol 51:205–211. https://doi.org/10.1111/j.1472-765X.2010.02883.x CrossRefPubMedGoogle Scholar
- 102.Jack RF, Ringelberg DB, White DC (1992) Differential corrosion rates of carbon steel by combinations of Bacillus sp., Hafnia alvei and Desulfovibrio gigas established by phospholipid analysis of electrode biofilm. Corros Sci 33:1843–1853. https://doi.org/10.1016/0010-938X(92)90188-9 CrossRefGoogle Scholar
- 109.Edwards JL, Smith DL, Connolly J, McDonald JE, Cox MJ, Joint I, Edwards C, McCarthy AJ (2010) Identification of carbohydrate metabolism genes in the metagenome of a marine biofilm community shown to be dominated by Gammaproteobacteria and Bacteroidetes. Genes 1:371–384. https://doi.org/10.3390/genes1030371 CrossRefPubMedPubMedCentralGoogle Scholar
- 115.Rogers TE (2005) Cellulase and hemicellulase activity within the Tipula abdominalis larval gut. Dissertation, University of GeorgiaGoogle Scholar