Biogeochemistry of dihydrogen (H2).

Abstract

Hydrogen has had an important and evolving role in Earth's geo- and biogeochemistry, from prebiotic to modern times. On the earliest Earth, abiotic sources of H2 were likely stronger than in the present. Volcanic out-gassing and hydrothermal circulation probably occurred at several times the modern rate, due to presumably higher heat flux. The H2 component of volcanic emissions was likely buffered close to the modern value by an approximately constant mantle oxidation state since 3.9 billion years ago, and may have been higher before that, if the early mantle was more reducing. The predominantly ultramafic character of the early, undifferentiated crust could have led to increased serpentinization and release of H2 by hydrothermal circulation, as in modern ultramafic-hosted vents. At the same time, the reactive atmospheric sink for H2 was likely weaker. Collectively, these factors suggest that steady state levels of H2 in the prebiotic atmosphere were 3-4 orders of magnitude higher than at present, and possibly higher still during transient periods following the delivery of Fe and Ni by large impact events. These elevated levels had direct or indirect impacts on the redox state of the atmosphere, the radiation budget, the production of aerosol hazes, and the genesis of biochemical precursor compounds. The early abiotic cycling of H2 helped to establish the environmental and chemical context for the origins of life on Earth. The potential for H2 to serve as a source of energy and reducing power, and to afford a means of energy storage by the establishment of proton gradients, could have afforded it a highly utilitarian role in the earliest metabolic chemistry. Some origin of life theories suggest the involvement of H2 in the first energy-generating metabolism, and the widespread and deeply-branching nature of H2-utilization in the modern tree of life suggests that it was at least a very early biochemical innovation. The abiotic production of H2 via several mechanisms of water-rock interaction could have supported an early chemosynthetic biosphere. Such processes offer the continued potential for a deep, rock-hosted biosphere on Earth or other bodies in the solar system. The continued evolution of metabolic and community-level versatility among microbes led to an expanded ability to completely exploit the energy available in complex organic matter. Under the anoxic conditions that prevailed on the early Earth, this was accomplished through the linked and sequential action of several metabolic classes of organisms. By transporting electrons between cells, H2 provides a means of linking the activities of these organisms into a highly functional and interactive network. At the same time, H2 concentrations exert a powerful thermodynamic control on many aspects of metabolism and biogeochemical function in these systems. Anaerobic communities based on the consumption of organic matter continue to play an important role in global biogeochemistry even into the present day. As the principal arbiters of chemistry in most aquatic sediments and animal digestive systems, these microbes affect the redox and trace-gas chemistry of our oceans and atmosphere, and constitute the ultimate biological filter on material passing into the rock record. It is in such communities that the significance of H2 in mediating biogeochemical function is most strongly expressed. The advent of phototrophic metabolism added another layer of complexity to microbial communities, and to the role of H2 therein. Anoxygenic and oxygenic phototrophs retained and expanded on the utilization of H2 in metabolic processes. Both groups produce and consume H2 through a variety of mechanisms. In the natural world, phototrophic organisms are often closely juxtaposed with a variety of other metabolic types, through the formation of biofilms and microbial mats. In the few examples studied, phototrophs contribute an often swamping term to the H2 economy of these communities, with important implications for their overall function-including regulation of the redox state of gaseous products, and direct release of large quantities of H2 to the environment. As one of the dominant sources of biological productivity for as much as 2 billion years of Earth's history, these communities have been among the most important agents of long-term global biogeochemical change. On the modern Earth, H2 is present at only trace levels in the atmosphere and oceans. Nonetheless, its function as an arbiter of microbial interactions and chemistry ensures an important role in biogeochemical cycling. The significance of H2 in a global sense may soon increase, as the search for alternative fuels casts attention on the clean-energy potential of hydrogen fuel cells. Already, H2 utilization plays an important role in all three phylogenetic domains of life. Humans may soon add an important new term to this economy. Considerable research is focused on the H2-producing capacities of phototrophic and other microorganisms as potential contributors in this regard. Regardless of source, the large scale utilization of H2 as an energy source could carry important consequences for biogeochemistry.