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.

Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria

“…This study also highlights the genomic plasticity of SUP05, which enables this widely distributed group to optimize its energy metabolism (electron donor and acceptor) to local geochemical conditions. Guaymas | oxygen minimum zone D eep-sea hydrothermal vent ecosystems depend on microorganisms that use reduced chemicals such as sulfur, methane, ammonium, and H 2 as electron donors for chemosynthesis (1)(2)(3)(4)(5). Recent work suggests that microbial chemosynthesis is also far more prevalent in the broader deep oceans than previously recognized, extending throughout the water column of the dark open ocean, where it serves as a significant source of organic carbon (6,7).…”

Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri

“…The hydrothermal vent mussels Bathymodiolus azoricus and B. puteoserpentis are nutritionally sustained by chemolithoautotrophic and methanotrophic endosymbionts (Duperron et al, 2006;Petersen et al, 2011). When 13 C enrichment was evaluated in 13 C-labelled bicarbonate tracer experiments using living B. azoricus individuals, the 13 C enrichment level in the gill containing thioautotrophic endosymbionts was the highest among all tissues, whereas the 13 C enrichment level of tissues, including the digestive system, was slightly higher compared with that of muscles (Riou et al, 2008).…”

A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage

“…Assuming that the Sisters Peak low-temperature fluids emanate at a rate as has been estimated for other venting sites and assuming that all the local Thiomicrospira species are active and consume hydrogen at the above mentioned rates then between 84 nmol (0.00002 kJ) and 105 mmol hydrogen (0.025 kJ) could be consumed and subsequently 17 nmol and 21 mmol CO 2 could be fixed at one venting site in 1 h by Thiomicrospira. For comparison, Petersen et al (2011) calculated that 435 mmol hydrogen could be consumed per hour by endosymbionts inhabiting a single vent mussel. The Sisters Peak endmember fluids-that is, 100% hydrothermal fluids without any mixed ambient seawater-holds an estimated 1.6 mM hydrogen (Perner et al, 2014).…”