Hydrogen as an energy source for hydrothermal vent symbioses

Both reduced sulphur and methane have previously been described as energy sources for symbiotic bacteria in marine chemosynthetic ecosystems. Though many other potential chemosynthetic sources are available, none have previously been shown to be utilised by such bacteria.  The interaction between mantle-derived ultramafic rocks and seawater at some hydrothermal vents produces fluids characterised by high hydrogen concentrations. With an energy yield from hydrogen oxidation providing 7 times and 18 times more energy kg¯¹ vent fluid than methane oxidation and sulphide oxidation respectively, hydrogen would be a favourable energy source for chemosynthetic microbes.

Mussels, Bathymodiolus puteoserpentis, are the most abundant macrofauna at the Logatchev vent field on the Mid-Atlantic Ridge, characterised by ultramafic outcrops. The gills of these mussels play host to methane and sulphur oxidising bacteria which allows them to dominate such an environment. Such bacteria have shown a genetic potential for hydrogen uptake and oxidation. Membrane-bound respiratory enzymes, NiFe hydrogenases, are key to hydrogen metabolism. The hupL gene, responsible for encoding NiFe hydrogenases, was found in gill tissues containing bacterial symbionts.  The presence of this gene was not limited to mussel symbionts at high hydrogen concentration vents however, with other vent mussels containing symbionts with hydrogen uptake properties. 

Upon incubation of B. puteoserpentis gill tissues with hydrogen, rapid-uptake of hydrogen was observed. Subsequent incubation with both hydrogen and CO₂ together determined that carbon uptake and fixation rates were comparable to fixation rates concurrent with sulphide, suggesting that carbon autotrophy could be fuelled by sulphide and hydrogen to the same extent. Utilisation of hydrogen as an additional energy source was also feasible though less efficient at low hydrogen venting systems with symbionts of mussels from such sites having the capacity to uptake hydrogen at a rate correlated with ambient concentration.

Of the two chemosynthetic gammaproteobacteria hosted in B. puteoserpentis gills, sulphur-oxidising and methane-oxidising, it was found that hydrogen is utilised by sulphur-oxidizing bacteria. Genome sequencing, hupL gene FISH and immunohistochemistry in conjunction with 16S rRNA FISH all inferred a link between hydrogen uptake and utilisation by sulphur-oxidising bacteria for energy.

To account for uncertainties in extrapolating data from laboratory-based manipulation experiments an in situ mass spectrometer was deployed to simultaneously measure hydrogen concentrations and temperature in two areas around vents: directly at the source of fluid emissions from the seafloor and an area where fluids had been exposed to a B. puteoserpentis mussel bed. Significant hydrogen depletion was measured around mussel beds in comparison to source fluid confirming a high consumption of hydrogen by mussel beds, probably by sulphur-oxidising bacteria. This trend was also true of methane.

It makes sense that with high hydrogen availability having the capacity to utilise hydrogen as a source of energy provides a competitive edge, and allows the occupancy of a different niche. Though not observed for methane symbionts in B. puteoserpentis, there is the potential for the utilisation hydrogen as energy source to be prevalent amongst other vents mussels and other symbiotic bacteria for chemosynthesis. If so, it could prove to be of huge environmental importance as a hydrogen sink.  

Petersen J., Zielinski F., Pape T., Sierfert R., Moraru C., Amann R., Hourdez S., Girguis P., Wankel S., Barbe V., Pelletier E., Fink D., Borowski C., Bach W. and Dubilier N. (2011) Hydrogen as an energy source for hydrothermal vent symbioses. Nature, 476, 176-180