Hydrothermal Vent Symbioses and Hydrogen: A Recently Discovered Source of Energy for Marine Chemosynthetic Ecosystems

Free-living, chemosynthetic, hydrothermal vent bacteria are known to utilise many energy sources, including ammonium, ferrous iron, hydrogen and manganese.  However until recently only two energy sources had been shown to fuel primary production in symbiotic bacteria crucial to the metazoans which inhabit hydrothermal vents: reduced sulphur compounds and methane. Yet the energy yield from hydrogen oxidation is much higher than that for the oxidation of methane or sulphur, making it a favourable election donor.  Furthermore, some hydrothermal vents produce fluids with very high hydrogen concentrations, due seawater interaction with mantle-derived rock; these vents also tend to have high methane concentrations and low hydrogen sulphide (H₂S) concentrations, whereas vents in basalt rock are characterised by fluids high in H₂S, and low in hydrogen and methane.  

Abundant, vent-inhabiting Bathymodiolus mussels host methane-oxidising and chemoautotrophic sulphur-oxidising bacteria in their gills; Peterson et al. (2011) investigated whether hydrogen was being used as an energy source in the autotrophy of these mussel symbionts. Hydrogen metabolism is known to involve enzymes which channel electrons from hydrogen, into the quinone pool, thus linking hydrogen oxidation to energy production; the large subunit of these key, membrane-bound, uptake hydrogenases are coded by the hupL gene.  The authors amplified and sequenced this gene from symbiont-containing gill-tissues of Bathymodiolus mussel species collected from both hydrogen-rich and hydrogen–poor vent sites, thus showing the genetic potential for hydrogen oxidation in symbionts from both types of vent.  Peterson et al. (2011) went on to examine the actual uptake of hydrogen by symbiont-containing mussel gill tissues.

The authors recorded rapid hydrogen consumption by symbiont-containing Bathymodiolus gills, in contrast to symbiont-free foot tissue, which matched other negative controls; additionally hydrogen consumption rates were found to be 20- to 30-fold lower in mussel gill tissue from hydrogen-poor sites compared to tissue from hydrogen-rich environments.  In order to confirm that hydrogen uptake was coupled to CO₂ fixation in Bathymodiolus symbionts, Peterson et al. (2011) incubated mussel gill tissues collected from a hydrogen-rich site, in seawater containing ¹⁴C-bicarbonate, with hydrogen, or with either sulphide or no electron source (controls).  Carbon fixation rates in mussel gill tissue incubated with hydrogen were comparable to those incubated with sulphide, suggesting that not only does hydrogen fuel autotrophy, providing energy for mussel biomass production, but that at hydrogen-rich sites, hydrogen is as important as sulphide in this process.

Lastly, as both sulphur-oxidising bacteria and methane-oxidising bacteria are known to be associated with Bathymodiolus, Peterson et al. (2011) explored which type of chemosynthetic symbiont was using hydrogen; symbiont Identity was linked to function via both DNA and protein based methods.   Metagenomic analysis revealed that a single genome fragment contained all the genetic components necessary for hydrogen uptake, alongside key genes for sulphur oxidation and CO₂ fixation, leading the authors to suggest that the fragment came from a sulphur-oxidising symbiont.    Via single-gene fluorescence in situ hybridisation (FISH), signals from hupL gene probes were observed to overlap 16S rRNA FISH signals from the same sulphur-oxidising symbiont, further implying that this symbiont uses hydrogen.  Finally, hydrogenase gene expression in the sulphur-reducing symbiont was confirmed via immunohistochemistry: anti-hydrogenase antibody signals were observed to overlap with sulphur-reducing symbiont 16S rRNA FISH signals in single Bathymodiolus gills cells; FISH signals from the methane-oxidising symbiont did not overlap.

The thorough nature of the authors’ investigation is persuasive as to the reality of hydrogen use in mussel biomass production at hydrothermal vents.  The environmental significance of H₂ use was also explored by Peterson et al. (2011):  temperature and hydrogen concentration of vent fluids that had crossed mussel beds were measured (via en situ mass spectrometry), as were vent fluids that had not been exposed to macrofauna; a significantly lower slope in the regression line of the former condition suggested that fluids in the mussel beds were hydrogen depleted.  The authors’ calculate that this level of hydrogen consumption may well make Bathymodiolus mussels a significant hydrogen sink; it is also proposed that hydrogen use may be widespread in chemoautotrophic symbiosis, such as those observed in tubeworms and shrimps, and that this may be especially important at hydrogen rich sites.  Further investigation of these theories appears warranted: a better comprehension of hydrogen as an energy source in hydrothermal vent symbioses may affect not only our understanding of how vent ecosystems function, but also of how the marine hydrogen cycle operates.

Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R, Hourdez S, et al. (2011) Hydrogen Is an Energy Source for Hydrothermal Vent Symbioses. Nature 476: 176–80.

http://www.nature.com/nature/journal/v476/n7359/full/nature10325.html