Abstract
ABSTRACTA chemolithoautotrophic strain of the family Beggiatoaceae, Beggiatoa sp. strain 35Flor, was found to oxidize molecular hydrogen when grown in a medium with diffusional gradients of oxygen, sulfide, and hydrogen. Microsensor profiles and rate measurements suggested that the strain oxidized hydrogen aerobically when oxygen was available, while hydrogen consumption under anoxic conditions was presumably driven by sulfur respiration. Beggiatoa sp. 35Flor reached significantly higher biomass in hydrogen-supplemented oxygen-sulfide gradient media, but hydrogen did not support growth of the strain in the absence of reduced sulfur compounds. Nevertheless, hydrogen oxidation can provide Beggiatoa sp. 35Flor with energy for maintenance and assimilatory purposes and may support the disposal of internally stored sulfur to prevent physical damage resulting from excessive sulfur accumulation. Our knowledge about the exposure of natural populations of Beggiatoaceae to hydrogen is very limited, but significant amounts of hydrogen could be provided by nitrogen fixation, fermentation, and geochemical processes in several of their typical habitats such as photosynthetic microbial mats and submarine sites of hydrothermal fluid flow.IMPORTANCE Reduced sulfur compounds are certainly the main electron donors for chemolithoautotrophic Beggiatoaceae, but the traditional focus on this topic has left other possible inorganic electron donors largely unexplored. In this paper, we provide evidence that hydrogen oxidation has the potential to strengthen the ecophysiological plasticity of Beggiatoaceae in several ways. Moreover, we show that hydrogen oxidation by members of this family can significantly influence biogeochemical gradients and therefore should be considered in environmental studies.
Highlights
A chemolithoautotrophic strain of the family Beggiatoaceae, Beggiatoa sp. strain 35Flor, was found to oxidize molecular hydrogen when grown in a medium with diffusional gradients of oxygen, sulfide, and hydrogen
This suggests that hydrogen oxidation may be a widespread metabolic trait among sulfur oxidizers and as such may be realized in the family Beggiatoaceae
Beggiatoa sp. 35Flor filaments grew in dense, opaque mats at the transition from oxic to sulfidic conditions when cultivated in agar-stabilized gradient media (Fig. 2)
Summary
A chemolithoautotrophic strain of the family Beggiatoaceae, Beggiatoa sp. strain 35Flor, was found to oxidize molecular hydrogen when grown in a medium with diffusional gradients of oxygen, sulfide, and hydrogen. Members of the family Beggiatoaceae are colorless sulfur bacteria known to oxidize reduced sulfur compounds and organic substances for chemolithoautotrophic, chemoorganoheterotrophic, and mixotrophic growth [1]. Hydrogen oxidation or hydrogen-supported growth has been reported for many other well-known sulfur oxidizers such as members of the families Chromatiaceae [8], Acidithiobacillaceae [9, 10], Aquificaceae [11,12,13], and Sulfolobaceae [14], the genus Sulfurimonas [15, 16], the SUP05 clade [17], and endosymbionts of mussels [18]. Culture-based experiments allowed us to adjust the concentrations of hydrogen and sulfide to levels at which reliable measurements with the hydrogen microsensor are
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