Diversity and metabolism of prokaryotic chemoautotrophs and their interactions with deep-sea hydrothermal environments

Abstract

The deep sea hydrothermal vent ecosystem was first discovered in 1977 at East Pacific Rise (EPR) near the Galapagos Islands. In the past decades, over 640 hydrothermal vent sites have been found in oceans, a majority of which have been found on the mid-ocean ridges. Chinese scientists have contributed significantly to the discovery of new sites on the Southwest Indian Ridge and South Mid-Atlantic Ridge. Due to worldwide oceanic expeditions, significant advances have been made in the observation of hydrothermal vent ecosystems, regarding the diversity and geographical distribution of vent fauna and microbial communities. The vent chemolithoautotrophs and their symbiosis with vent clams, mussels, tube worms and shrimps, in particular, gained more attention. In this paper, recent advances in diversity and versatile metabolisms of prokaryotic chemoautotrophs are reviewed. The vent chemolithoautotrophs are pivotal in the cross-connected interactions of abiotic and biotic processes. They act as the primary producer in the unique ecosystem driven by the deep dark energy derived from water-rock reaction around the magma chamber. Correspondingly, various chemoautotrophic bacteria are capable of utilizing the reduced compounds generated by water-rock reaction, via sulfur oxidization, methane oxidization, hydrogen oxidization, iron oxidization and ammonia oxidization; in contrast, chemoautotrophic vent archaea tend to harness energy from hydrogen in the inner part of the hydrothermal chimney coupling with sulfur reduction. In addition, heterotrophic archaea of Thermococcales also frequently occurs in high temperature chimneys; while some archaea can oxidize ammonia and methane in the vent surroundings. These diverse prokaryotes selectively distribute in a variety of vent niches along the steep environmental gradients of temperature, pH, Eh and concentrations of the reduced compounds. In the case of a black smoke ecosystem, where the hydrogen sulfide in hydrothermal fluids is effluent, sulfur oxidation is recognized as a major process driving carbon fixation for primary production; while in the mixing zones, the partially oxidized inorganic sulfur compounds like thiosulfate and polysulfide can be further oxidized by sulfur-oxidizing bacteria (SOB). Among them, Epsilonproteobacteria such as Sulfurimonas, Sulfurovum, Arcobacter , Hydrogenovibrio and Thiomicrospira are predominant genera of SOBs in plume-mixed seawater close to the vent, while bacteria of Gammaproteobacteria SUP05 clade are relatively abundant in the cold oxidized seawater farther away from the vent. In the case of the white chimney, methane-metabolizing archaea of Methanosarcinales and hydrogen- oxidizing Thiomicrospira dominate the prokaryotic community in microbial mat. In addition, another group of chemolithoautotrophs function as endo- and epi-symbionts of vent animals that are essential to the health of vent ecosystem; these symbionts mostly belong to sulfur, hydrogen and methane oxidizers. However, all these processes need quantification to evaluate the efflux of energy and synthesized organic compounds. Considering the global distribution and the immense influence in respect to continuous efflux of energy and substances, hydrothermal vents play an important role in life evolution. Both geological records and computational analysis reveal that early life on Earth is likely originated from the deep hydrothermal system, with features of anaerobic, thermophilic, hydrogen-oxidizing, coupled with carbon and nitrogen fixation, represented by the Last Universal Common Ancestor (LUCA). Because of our limited knowledge about the deep biosphere along with deep time evolution, more efforts are needed to investigate the dark ecosystem with integrated approaches, to project the nature of life in dark with unique mechanisms, and to finally elucidate the origin and evolution of life on earth.