Hydrogen is an energy source for hydrothermal vent symbioses

Abstract

The discovery of deep-sea hydrothermal vents in 1977 revolutionized our understanding of the energy sources that fuel primary productivity on Earth. Hydrothermal vent ecosystems are dominated by animals that live in symbiosis with chemosynthetic bacteria. So far, only two energy sources have been shown to power chemosynthetic symbioses: reduced sulphur compounds and methane. Using metagenome sequencing, single-gene fluorescence in situ hybridization, immunohistochemistry, shipboard incubations and in situ mass spectrometry, we show here that the symbionts of the hydrothermal vent mussel Bathymodiolus from the Mid-Atlantic Ridge use hydrogen to power primary production. In addition, we show that the symbionts of Bathymodiolus mussels from Pacific vents have hupL, the key gene for hydrogen oxidation. Furthermore, the symbionts of other vent animals such as the tubeworm Riftia pachyptila and the shrimp Rimicaris exoculata also have hupL. We propose that the ability to use hydrogen as an energy source is widespread in hydrothermal vent symbioses, particularly at sites where hydrogen is abundant.

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Figure 1: Hydrogen consumption in Bathymodiolus gills.
Figure 2: The sulphur-oxidizing symbiont has the gene for hydrogen uptake, which it expresses.
Figure 3: Hydrogen is consumed in mussel beds of B. puteoserpentis.

Accession codes

Data deposits

All hupL sequences have been deposited at NCBI under accession numbers FR851255–FR851274. The sequences that make up the genome fragment and the RAST annotation can be found at NCBI under project identification 65421 (accession numbers CAEB01000001–CAEB01000078).

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Acknowledgements

We thank the chief scientists, and the captains and crews of the research vessels and remotely operated vehicles involved in sampling and analyses at sea. Thank you to D. Garbe-Schönberg, K. van der Heijden and J. Stecher for on-board sampling and analysis, and S. Duperron, M.-A. Cambon-Bonavita and M. Zbinden for providing samples. We acknowledge B. Friedrich and O. Lenz for the antiserum against the C. necator uptake hydrogenase, J. Milucka for help with western blots and T. Holler for culturing C. necator. S. Wetzel provided technical assistance. This work was supported by the German Science Foundation (DFG) Priority Program 1144 “From Mantle to Ocean: Energy-, Material- and Life Cycles at Spreading Axes” (publication number 60), the DFG Cluster of Excellence “The Ocean in the Earth System” at MARUM (Center for Marine Environmental Sciences), and the Max Planck Society.

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J.M.P., F.U.Z., T.P., R.S., C.B., D.F. and N.D. did the on-board experiments during the research cruises. F.U.Z. analysed the data from physiology experiments. J.M.P. amplified and sequenced hupL, analysed the genome data, did western blots and immunohistochemistry. C.M. and R.A. did the geneFISH. S.H., S.D.W. and P.R.G. did the in situ mass spectrometry and analysed the data. V.B. and E.P. did the genome sequencing and assembly. W.B. did the thermodynamic modelling. J.M.P., F.U.Z. and N.D. conceived the study and wrote the paper.

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Correspondence to Nicole Dubilier.

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Petersen, J., Zielinski, F., Pape, T. et al. Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180 (2011). https://doi.org/10.1038/nature10325

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