Abstract
BackgroundSurface waters of aquatic environments have been shown to both evolve and consume hydrogen and the ocean is estimated to be the principal natural source. In some marine habitats, H2 evolution and uptake are clearly due to biological activity, while contributions of abiotic sources must be considered in others. Until now the only known biological process involved in H2 metabolism in marine environments is nitrogen fixation.Principal FindingsWe analyzed marine and freshwater environments for the presence and distribution of genes of all known hydrogenases, the enzymes involved in biological hydrogen turnover. The total genomes and the available marine metagenome datasets were searched for hydrogenase sequences. Furthermore, we isolated DNA from samples from the North Atlantic, Mediterranean Sea, North Sea, Baltic Sea, and two fresh water lakes and amplified and sequenced part of the gene encoding the bidirectional NAD(P)-linked hydrogenase. In 21% of all marine heterotrophic bacterial genomes from surface waters, one or several hydrogenase genes were found, with the membrane-bound H2 uptake hydrogenase being the most widespread. A clear bias of hydrogenases to environments with terrestrial influence was found. This is exemplified by the cyanobacterial bidirectional NAD(P)-linked hydrogenase that was found in freshwater and coastal areas but not in the open ocean.SignificanceThis study shows that hydrogenases are surprisingly abundant in marine environments. Due to its ecological distribution the primary function of the bidirectional NAD(P)-linked hydrogenase seems to be fermentative hydrogen evolution. Moreover, our data suggests that marine surface waters could be an interesting source of oxygen-resistant uptake hydrogenases. The respective genes occur in coastal as well as open ocean habitats and we presume that they are used as additional energy scavenging devices in otherwise nutrient limited environments. The membrane-bound H2-evolving hydrogenases might be useful as marker for bacteria living inside of marine snow particles.
Highlights
The composition of earth’s atmosphere is the result of a number of concurring processes and a matter of continuous change
A search of genebank and cyanobase for all available cyanobacterial sequences revealed the presence of the bidirectional NAD(P)-linked hydrogenase in all the freshwater strains and all the strains isolated from microbial mats, salt marshes, and the intertidal zone (Table 2)
For several reasons described in detail below, we think that biological hydrogen production and consumption, as depicted in Fig. 6, might be common in a large number of marine and freshwater habitats
Summary
The composition of earth’s atmosphere is the result of a number of concurring processes and a matter of continuous change. Hydrogen is the second most abundant trace gas in the atmosphere, making up around 0.5 ppm to 0.6 ppm [1,2]. 90% of hydrogen evolution is due to photochemical oxidation of hydrocarbons such as methane in the atmosphere, the combustion of fossil fuels and biomass burning. Natural evolution results from volcanic activity, the nitrogen fixation process in legumes and an uncharacterized source in the oceans. The latter comprises the majority with around 6% (6 Tg per year [3]). Until now the only known biological process involved in H2 metabolism in marine environments is nitrogen fixation
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