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Biodegradation as an important sink of aromatic hydrocarbons in the oceans

Nature Geoscience volume 12, pages 119–125 (2019)Cite this article

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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.

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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.

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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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Authors and Affiliations

  1. Department of Environmental Chemistry, Institute of Environmental Assessment and Water Research, IDAEA-CSIC, Barcelona, Spain

    Belén González-Gaya, Alicia Martínez-Varela, Maria Vila-Costa, Paulo Casal, Elena Cerro-Gálvez, Naiara Berrojalbiz & Jordi Dachs

  2. Department of Instrumental Analysis and Environmental Chemistry, Institute of Organic Chemistry, IQOG-CSIC, Madrid, Spain

    Belén González-Gaya & Begoña Jiménez

  3. Centre for Ecology and Evolution in Microbial Model Systems, EEMiS, Linnaeus University, Kalmar, Sweden

    Daniel Lundin

  4. Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Barcelona, Spain

    Montserrat Vidal

  5. Spanish Oceanography Institute, IEO, Oceanographic Centre of A Coruña, A Coruña, Spain

    Carmen Mompeán & Antonio Bode

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  1. Belén González-Gaya
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Contributions

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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