Abstract
Filamentous large sulfur-oxidizing bacteria (FLSB) of the family Beggiatoaceae are globally distributed aquatic bacteria that can control geochemical fluxes from the sediment to the water column through their metabolic activity. FLSB mats from hydrothermal sediments of Guaymas Basin, Mexico, typically have a "fried-egg" appearance, with orange filaments dominating near the center and wider white filaments at the periphery, likely reflecting areas of higher and lower sulfide fluxes, respectively. These FLSB store large quantities of intracellular nitrate that they use to oxidize sulfide. By applying a combination of 15N-labeling techniques and genome sequence analysis, we demonstrate that the white FLSB filaments were capable of reducing their intracellular nitrate stores to both nitrogen gas and ammonium by denitrification and dissimilatory nitrate reduction to ammonium (DNRA), respectively. On the other hand, our combined results show that the orange filaments were primarily capable of DNRA. Microsensor profiles through a laboratory-incubated white FLSB mat revealed a 2- to 3-mm vertical separation between the oxic and sulfidic zones. Denitrification was most intense just below the oxic zone, as shown by the production of nitrous oxide following exposure to acetylene, which blocks nitrous oxide reduction to nitrogen gas. Below this zone, a local pH maximum coincided with sulfide oxidation, consistent with nitrate reduction by DNRA. The balance between internally and externally available electron acceptors (nitrate) and electron donors (reduced sulfur) likely controlled the end product of nitrate reduction both between orange and white FLSB mats and between different spatial and geochemical niches within the white FLSB mat.IMPORTANCE Whether large sulfur bacteria of the family Beggiatoaceae reduce NO3- to N2 via denitrification or to NH4+ via DNRA has been debated in the literature for more than 25 years. We resolve this debate by showing that certain members of the Beggiatoaceae use both metabolic pathways. This is important for the ecological role of these bacteria, as N2 production removes bioavailable nitrogen from the ecosystem, whereas NH4+ production retains it. For this reason, the topic of environmental controls on the competition for NO3- between N2-producing and NH4+-producing bacteria is of great scientific interest. Recent experiments on the competition between these two types of microorganisms have demonstrated that the balance between electron donor and electron acceptor availability strongly influences the end product of NO3- reduction. Our results suggest that this is also the case at the even more fundamental level of enzyme system regulation within a single organism.
Highlights
IMPORTANCE Whether large sulfur bacteria of the family Beggiatoaceae reduce NO3Ϫ to N2 via denitrification or to NH4ϩ via dissimilatory nitrate reduction to ammonium (DNRA) has been debated in the literature for more than 25 years
We demonstrated that lab-incubated white filamentous large sulfuroxidizing bacteria (FLSB) mats from Guaymas Basin can reduce NO3Ϫ to both N2 via denitrification and to NH4ϩ via DNRA (Fig. 1 and Table 1)
We further showed that the bulk turnover in both denitrification and DNRA could be attributed to the FLSB filaments and not the smaller mat-associated microorganisms
Summary
Maximum N2O production occurred at a depth of around 1 mm inside the mat, just below the zone where O2 disappeared (Fig. 2b). N2O production in white FLSB mats was investigated in batch incubations. These mats produced N2O after acetylene was added, and N2O production ceased after the FLSB filaments were destroyed (see Fig. S4 in the supplemental material). The genome from unpigmented white Guaymas Basin filaments [16] (Fig. 3) has almost-complete sets of genes for both DNRA and denitrification (Table 2). Vacuole that took up most of the cell volume in the multicellular wide white filaments (Fig. 3b and c)
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