Abstract

Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deep-sea microbial food webs and impact the biogeochemical cycling of carbon and other elements is unclear. Hydrostatic pressure (HP) is a distinctive parameter of the deep sea, although rarely investigated. Whether HP alone affects the assembly and activity of oil-degrading communities remains to be resolved. Here we have demonstrated that hydrocarbon degradation in deep-sea microbial communities is lower at native HP (10 MPa, about 1000 m below sea surface level) than at ambient pressure. In long-term enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of beta-oxidation-related proteins (i.e., the main hydrocarbon-degradation pathway) resulting in low cell growth and CO2 production. Short-term experiments with HP-adapted synthetic communities confirmed this data, revealing a HP-dependent accumulation of citrate and dihydroxyacetone. Citrate accumulation suggests rates of aerobic oxidation of fatty acids in the TCA cycle were reduced. Dihydroxyacetone is connected to citrate through glycerol metabolism and glycolysis, both upregulated with increased HP. High degradation rates by obligate hydrocarbon-degraders may thus be unfavourable at increased HP, explaining their selective suppression. Through lab-scale cultivation, the present study is the first to highlight a link between impaired cell metabolism and microbial community assembly in hydrocarbon degradation at high HP. Overall, this data indicate that hydrocarbons fate differs substantially in surface waters as compared to deep-sea environments, with in situ low temperature and limited nutrients availability expected to further prolong hydrocarbons persistence at deep sea.

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Acknowledgements

These findings were financially supported by the FP7-EU project Kill Spill (312139), the Geconcentreerde Onderzoeksactie, Ghent University (BOF15/GOA/006), the Danish Ministry of Higher Education and Science (AU-2010-612-181) and The Novonordisk Foundation (NNF16OC0021110). F.-M.K. was supported by the Inter-University Attraction Pole ‘μ-manager’ (BELSPO, P7/25). A.S. thanks Dr. Ann Vanreusel (Ghent University, Belgium) for her supervision during deep-sea sampling. Dr. Xiao Xiang and Yu Zhang (Shanghai Jiao Tong University, China) are acknowledged for their assistance with high-pressure reactors. A. Bastian (Otto von Guericke University of Magdeburg) and Katrine Bay Jensen (Aarhus University) are acknowledged for their technical assistance.

Author contributions

A.S. conceived, designed and performed the experiments, and wrote the manuscript. R.H. performed the metaproteome analyses and co-wrote the manuscript. C.D. performed the metaproteome analyses. R.R. performed the experiments at high pressure and isolation of the micro-colonies. F.-M.K. performed the 16S rRNA analyses. I.M.B. performed the statistical analysis and the sequencing of the isolates. A.M. co-wrote the manuscript. P.V. analysed the amino acid data. H.B. and F.M. analysed the PLFA data. I.M.B. performed surfactants analysis and general editing. K.M. and T.V. analysed intracellular compounds. D.B. performed the metaproteome data analysis. U.R. supervised the metaproteome analysis. N.B. funded and supervised the project. All authors reviewed the manuscripts.

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Affiliations

  1. Center for Microbial Ecology and Technology (CMET), Gent University, Coupure Links 653, Gent, B 9000, Belgium

    • Alberto Scoma
    • , Ridwan Rifai
    • , Frederiek-Maarten Kerckhof
    •  & Nico Boon
  2. Department of Bioscience, Microbiology Section, Aarhus University, Ny Munkegade 116, Aarhus C, 8000, Denmark

    • Alberto Scoma
    • , Ian Marshall
    •  & Angeliki Marietou
  3. Biological and Chemical Engineering, Aarhus University, Hangøvej 2, Aarhus N, 8200, Denmark

    • Alberto Scoma
  4. Otto von Guericke University of Magdeburg, Bioprocess Engineering, Universitätsplatz 2 G25, Magdeburg, 39106, Germany

    • Robert Heyer
    • , Christian Dandyk
    •  & Dirk Benndorf
  5. Department of Biotechnology, Delft University of Technology, Van der Maasweg 9, Delft, 2629HZ, The Netherlands

    • Henricus T. S. Boshker
    •  & Filip J. R. Meysman
  6. Department of Biology, University of Antwerp, Universiteitsplein 1, Wilrijk (Antwerp), BE- 2610, Belgium

    • Henricus T. S. Boshker
    •  & Filip J. R. Meysman
  7. Department of Analytical, Environmental and Geochemistry (AMGC), Vrije Univeriteit Brussel (VUB), Pleinlaan 2, Brussel, 1050, Belgium

    • Filip J. R. Meysman
  8. iNANO, Department of Chemistry, Aarhus University, Gustav Wieds vej 14, Aarhus C, 8000, Denmark

    • Kirsten G. Malmos
    •  & Thomas Vosegaard
  9. Laboratory for Chemical Analyses (LCA), Department of Green Chemistry and Technology, Gent University, Valentin Vaerwyckweg 1, Ghent, 9000, Belgium

    • Pieter Vermeir
  10. School of Biomedical Sciences, University of Ulster, Coleraine, N. Ireland, UK

    • Ibrahim M. Banat
  11. Max Planck Institute for Dynamics of Complex Technical Systems, Bioprocess Engineering, Sandtorstraße 1, Magdeburg, 39106, Germany

    • Dirk Benndorf

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Correspondence to Alberto Scoma.

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https://doi.org/10.1038/s41396-018-0324-5