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Biodegradation as an important sink of aromatic hydrocarbons in the oceans

Abstract

Atmospheric deposition of semivolatile aromatic hydrocarbons accounts for an important input of organic matter to the surface ocean. Nevertheless, the biogeochemical cycling and sinks of semivolatile aromatic hydrocarbons in the ocean remain largely uncharacterized. Here we present measurements of 64 polycyclic aromatic hydrocarbons in plankton and seawater from the Atlantic, Pacific, Indian and Southern Oceans, as well an assessment of their microbial degradation genes. Concentrations of the more hydrophobic compounds decreased when the plankton biomass was higher, consistent with the relevance of the biological pump. The mass balance for the global oceans showed that the settling fluxes of aromatic hydrocarbons in the water column were two orders of magnitude lower than the atmospheric deposition fluxes. This imbalance was high for low molecular weight hydrocarbons, such as phenanthrene and methylphenanthrenes, highly abundant in the dissolved phase. Parent polycyclic aromatic hydrocarbons were depleted to a higher degree than alkylated polycyclic aromatic hydrocarbons, and the degradation genes for polycyclic aromatic hydrocarbons were found to be ubiquitous in oceanic metagenomes. These observations point to a key role of biodegradation in depleting the bioavailable dissolved hydrocarbons and to the microbial degradation of atmospheric inputs of organic matter as a relevant process for the marine carbon cycle.

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Fig. 1: Global distribution of PAHs in the oceans.
Fig. 2: PAH profiles in the oceans.
Fig. 3: Cplankton relationships with biomass (B) and the fitted slope versus KOW.
Fig. 4: Mass balance of PAHs (black) and SALCs (red) for the surface Pacific, Atlantic and Indian Oceans (0–200 m).
Fig. 5: Frequencies of PAH degradation genes in the global oceans.

Data availability

The data sets generated during and/or analysed during the current study are included in this article (and Supplementary Information), or are available from the corresponding author on reasonable request.

References

  1. Zhang, Y. & Tao, S. Global atmospheric emission inventory of polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos. Environ. 43, 812–819 (2009).

    Article  Google Scholar 

  2. Wilcke, W. Global patterns of polycyclic aromatic hydrocarbons (PAHs) in soil. Geoderma 141, 157–166 (2007).

    Article  Google Scholar 

  3. Reddy, C. M. et al. Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proc. Natl Acad. Sci. USA 109, 20229–20234 (2012).

    Article  Google Scholar 

  4. Harvey, R. G. Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity (CUP Archive, Cambridge, 1991).

  5. Douben, P. E. PAHs: An Ecotoxicological Perspective (John Wiley & Sons, Chichester, 2003).

  6. Hylland, K. Polycyclic aromatic hydrocarbon (PAH) ecotoxicology in marine ecosystems. J. Toxicol. Environ. Health A 69, 109–123 (2006).

    Article  Google Scholar 

  7. Fernández-Pinos, M.-C. et al. Dysregulation of photosynthetic genes in oceanic Prochlorococcus populations exposed to organic pollutants. Sci. Rep. 7, 8029 (2017).

    Article  Google Scholar 

  8. González-Gaya, B. et al. High atmosphere–ocean exchange of semivolatile aromatic hydrocarbons. Nat. Geosci. 9, 438–442 (2016).

    Article  Google Scholar 

  9. Farrington, J. W. & Quinn, J. G. ‘Unresolved Complex Mixture’ (UCM): a brief history of the term and moving beyond it. Mar. Pollut. Bull. 96, 29–31 (2015).

    Article  Google Scholar 

  10. Ma, Y. et al. Deposition of polycyclic aromatic hydrocarbons in the North Pacific and the Arctic. J. Geophys. Res. Atmos. 118, 5822–5829 (2013).

    Article  Google Scholar 

  11. Castro-Jiménez, J., Berrojalbiz, N., Wollgast, J. & Dachs, J. Polycyclic aromatic hydrocarbons (PAHs) in the Mediterranean Sea: atmospheric occurrence, deposition and decoupling with settling fluxes in the water column. Environ. Pollut. 166, 40–47 (2012).

    Article  Google Scholar 

  12. Farrington, J. W. & Takada, H. Persistent organic pollutants (POPs), polycyclic aromatic hydrocarbons (PAHs), and plastics: examples of the status, trend, and cycling of organic chemicals of environmental concern in the ocean. Oceanography 27, 196–213 (2014).

    Article  Google Scholar 

  13. Dachs, J., Bayona, J. M., Fowler, S. W., Miquel, J.-C. & Albaigés, J. Vertical fluxes of polycyclic aromatic hydrocarbons and organochlorine compounds in the western Alboran Sea (southwestern Mediterranean). Mar. Chem. 52, 75–86 (1996).

    Article  Google Scholar 

  14. Deyme, R. et al. Vertical fluxes of aromatic and aliphatic hydrocarbons in the northwestern Mediterranean Sea. Environ. Pollut. 159, 3681–3691 (2011).

    Article  Google Scholar 

  15. Halsall, C. J., Sweetman, A. J., Barrie, L. A. & Jones, K. C. Modelling the behaviour of PAHs during atmospheric transport from the UK to the Arctic. Atmos. Environ. 35, 255–267 (2001).

    Article  Google Scholar 

  16. Nizzetto, L. et al. PAHs in air and seawater along a North–South Atlantic transect: trends, processes and possible sources. Environ. Sci. Technol. 42, 1580–1585 (2008).

    Article  Google Scholar 

  17. Lohmann, R. et al. Organochlorine pesticides and PAHs in the surface water and atmosphere of the North Atlantic and Arctic Ocean. Environ. Sci. Technol. 43, 5633–5639 (2009).

    Article  Google Scholar 

  18. Lohmann, R. et al. PAHs on a west-to-east transect across the tropical Atlantic Ocean. Environ. Sci. Technol. 47, 2570–2578 (2013).

    Article  Google Scholar 

  19. Dachs, J., Bayona, J. M., Raoux, C. & Albaigés, J. Spatial, vertical distribution and budget of polycyclic aromatic hydrocarbons in the western Mediterranean seawater. Environ. Sci. Technol. 31, 682–688 (1997).

    Article  Google Scholar 

  20. Berrojalbiz, N. et al. Biogeochemical and physical controls on concentrations of polycyclic aromatic hydrocarbons in water and plankton of the Mediterranean and Black Seas. Global Biogeochem. Cy. 25, GB4003 (2011).

    Article  Google Scholar 

  21. Bouloubassi, I. et al. PAH transport by sinking particles in the open Mediterranean Sea: a 1 year sediment trap study. Mar. Pollut. Bull. 52, 560–571 (2006).

    Article  Google Scholar 

  22. Adhikari, P. L., Maiti, K. & Overton, E. B. Vertical fluxes of polycyclic aromatic hydrocarbons in the northern Gulf of Mexico. Mar. Chem. 168, 60–68 (2015).

    Article  Google Scholar 

  23. Head, I. M., Jones, D. M. & Röling, W. F. M. Marine microorganisms make a meal of oil. Nat. Rev. Microbiol. 4, 173–182 (2006).

    Article  Google Scholar 

  24. Mallick, S., Chakraborty, J. & Dutta, T. K. Role of oxygenases in guiding diverse metabolic pathways in the bacterial degradation of low-molecular-weight polycyclic aromatic hydrocarbons: a review. Crit. Rev. Microbiol. 37, 64–90 (2011).

    Article  Google Scholar 

  25. Kimes, N. E., Callaghan, A. V., Suflita, J. M. & Morris, P. J. Microbial transformation of the Deepwater Horizon oil spill—past, present, and future perspectives. Front. Microbiol. 5, 603 (2014).

    Article  Google Scholar 

  26. Cerniglia, C. E. in Microorganisms to Combat Pollution (ed. Rosenberg, E.) 227–244 (Springer, Dordrecht, 1992).

  27. Peng, R.-H. et al. Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol. Rev. 32, 927–955 (2008).

    Article  Google Scholar 

  28. Seo, J.-S., Keum, Y.-S. & Li, Q. Bacterial degradation of aromatic compounds. Int. J. Environ. Res. Public Health 6, 278–309 (2009).

    Article  Google Scholar 

  29. Moody, J. D., Freeman, J. P., Doerge, D. R. & Cerniglia, C. E. Degradation of phenanthrene and anthracene by cell suspensions of Mycobacterium sp. strain PYR-1. Appl. Environ. Microbiol. 67, 1476–1483 (2001).

    Article  Google Scholar 

  30. Iwai, S., Johnson, T. A., Chai, B., Hashsham, S. A. & Tiedje, J. M. Comparison of the specificities and efficacies of primers for aromatic dioxygenase gene analysis of environmental samples. Appl. Environ. Microbiol. 77, 3551–3557 (2011).

    Article  Google Scholar 

  31. Brezna, B., Khan, A. A. & Cerniglia, C. E. Molecular characterization of dioxygenases from polycyclic aromatic hydrocarbon-degrading Mycobacterium spp. FEMS Microbiol. Lett. 223, 177–183 (2003).

    Article  Google Scholar 

  32. Kanaly, R. A. & Harayama, S. Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microb. Biotechnol. 3, 136–164 (2010).

    Article  Google Scholar 

  33. Mason, O. U. et al. Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J. 6, 1715–1727 (2012).

    Article  Google Scholar 

  34. Gallego, S. et al. Community structure and PAH ring-hydroxylating dioxygenase genes of a marine pyrene-degrading microbial consortium. Biodegradation 25, 543–556 (2014).

    Article  Google Scholar 

  35. Dombrowski, N. et al. Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill. Nat. Microbiol. 1, 16057 (2016).

    Article  Google Scholar 

  36. Liu, J. et al. Rapid response of eastern Mediterranean deep sea microbial communities to oil. Sci. Rep. 7, 5762 (2017).

    Article  Google Scholar 

  37. Rivers, A. R. et al. Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill. ISME J. 7, 2315 (2013).

    Article  Google Scholar 

  38. Siegel, D. A. Global assessment of ocean carbon export by combining satellite observations and food-web models. Global Biogeochem. Cy. 28, 181–196 (2014).

    Article  Google Scholar 

  39. Tsapakis, M., Apostolaki, M., Eisenreich, S. & Stephanou, E. G. Atmospheric deposition and marine sedimentation fluxes of polycyclic aromatic hydrocarbons in the eastern Mediterranean basin. Environ. Sci. Technol. 40, 4922–4927 (2006).

    Article  Google Scholar 

  40. Galbán-Malagón, C., Berrojalbiz, N., Ojeda, M. J. & Dachs, J. The oceanic biological pump modulates the atmospheric transport of persistent organic pollutants to the Arctic. Nat. Commun. 3, 862 (2012).

    Article  Google Scholar 

  41. Dachs, J. & Eisenreich, S. J. Adsorption onto aerosol soot carbon dominates gas-particle partitioning of polycyclic aromatic hydrocarbons. Environ. Sci. Technol. 34, 3690–3697 (2000).

    Article  Google Scholar 

  42. Bagby, S. C., Reddy, C. M., Aeppli, C., Fisher, G. B. & Valentine, D. L. Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon. Proc. Natl Acad. Sci. USA 114, E9–E18 (2017).

    Article  Google Scholar 

  43. Radović, J. R. et al. Assessment of photochemical processes in marine oil spill fingerprinting. Mar. Pollut. Bull. 79, 268–277 (2014).

    Article  Google Scholar 

  44. Berrojalbiz, N. et al. Accumulation and cycling of polycyclic aromatic hydrocarbons in zooplankton. Environ. Sci. Technol. 43, 2295–2301 (2009).

    Article  Google Scholar 

  45. Mende, D. R., Sunagawa, S., Zeller, G. & Bork, P. Accurate and universal delineation of prokaryotic species. Nat. Methods 10, 881–884 (2013).

    Article  Google Scholar 

  46. Ferraro, D. J., Okerlund, A. L., Mowers, J. C. & Ramaswamy, S. Structural basis for regioselectivity and stereoselectivity of product formation by naphthalene 1,2-dioxygenase. J. Bacteriol. 188, 6986–6994 (2006).

    Article  Google Scholar 

  47. Ferraro, D. J., Gakhar, L. & Ramaswamy, S. Rieske business: structure–function of Rieske non-heme oxygenases. Biochem. Biophys. Res. Commun. 338, 175–190 (2005).

    Article  Google Scholar 

  48. Gibson, D. T. & Parales, R. E. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr. Opin. Biotechnol. 11, 236–243 (2000).

    Article  Google Scholar 

  49. Kauppi, B. et al. Structure of an aromatic-ring-hydroxylating dioxygenase—naphthalene 1,2-dioxygenase. Structure 6, 571–586 (1998).

    Article  Google Scholar 

  50. Duarte, C. M., Regaudie-de-Gioux, A., Arrieta, J. M., Delgado-Huertas, A. & Agustí, S. The oligotrophic ocean is heterotrophic. Annu. Rev. Mar. Sci. 5, 551–569 (2013).

    Article  Google Scholar 

  51. Mompeán, C. et al. The influence of nitrogen inputs on biomass and trophic structure of ocean plankton: a study using biomass and stable isotope size-spectra. J. Plankton Res. 38, 1163–1177 (2016).

    Article  Google Scholar 

  52. Morales, L. et al. Oceanic sink and biogeochemical controls on the accumulation of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in plankton. Environ. Sci. Technol. 49, 13853–13861 (2015).

    Article  Google Scholar 

  53. Dachs, J. et al. Oceanic biogeochemical controls on global dynamics of persistent organic pollutants. Environ. Sci. Technol. 36, 4229–4237 (2002).

    Article  Google Scholar 

  54. Finn, R. D. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279–D285 (2015).

    Article  Google Scholar 

  55. Pesant, S. et al. Open science resources for the discovery and analysis of Tara Oceans data. Sci. Data 2, 150023 (2015).

    Article  Google Scholar 

  56. Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article  Google Scholar 

  57. Manor, O. & Borenstein, E. MUSiCC: a marker genes based framework for metagenomic normalization and accurate profiling of gene abundances in the microbiome. Genome. Biol. 16, 53 (2015).

    Article  Google Scholar 

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Acknowledgements

The authors thank the support of the RV Hespérides staff and UTM technicians during the cruise and Antarctic campaign. G. Caballero and M. J. Ojeda are acknowledged for technical support during the extraction and processing of the samples. This work was funded by the Spanish Government through the Malaspina 2010 (CSD2008-00077), REMARCA (CTM2012-34673), SENTINEL (CTM2015-70535-P) and ISOMICS (CTM2015-65691-R) projects. M.V.-C. acknowledges a Leonardo award from BBVA Foundation. Predoctoral fellowships from the Spanish government (A.M.-V. and P.C.), Catalan government (E.C.-G.), Spanish Oceanography Institute (C.M.) and BBVA Foundation (B.G.-G.) are acknowledged. B.G.-G., A.M.-V., M.V.-C., P.C., E.C.-G., N.B. and J.D. belong to the “Global Change and Genomic Biogeochemistry” research group funded by the Catalan Government (2017SGR800).

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B.G.-G., M.V.-C. and J.D. designed the work and wrote the manuscript. B.G.-G., P.C., B.J. and J.D. participated in the sampling campaigns. B.G.-G. and P.C. analysed the PAHs. B.G.-G., A.M.-V., M.V.-C., P.C., E.C.-G., N.B., B.J. and J.D. performed the fate assessment. A.M.-V., M.V.-C., E.C.-G. and D.L. did the bioinformatics work. C.M. and A.B. measured the carbon and nitrogen composition of the plankton samples. M.V. measured the organic carbon in the surface particulates. All the authors commented on the discussion and final version of the manuscript.

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Correspondence to Jordi Dachs.

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Supplementary Description, Supplementary Figures 1–7, Supplementary Tables 1–11

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González-Gaya, B., Martínez-Varela, A., Vila-Costa, M. et al. Biodegradation as an important sink of aromatic hydrocarbons in the oceans. Nature Geosci 12, 119–125 (2019). https://doi.org/10.1038/s41561-018-0285-3

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