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Bo Barker Jorgensen - One of the best experts on this subject based on the ideXlab platform.
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Motility patterns of filamentous sulfur bacteria, Beggiatoa spp.
FEMS microbiology ecology, 2011Co-Authors: Rita Dunker, Anja Kamp, Hans Røy, Bo Barker JorgensenAbstract:The large sulfur bacteria, Beggiatoa spp., live on the oxidation of sulfide with oxygen or nitrate, but avoid high concentrations of both sulfide and oxygen. As gliding filaments, they rely on reversals in the gliding direction to find their preferred environment, the oxygen–sulfide interface. We observed the chemotactic patterns of single filaments in a transparent agar medium and scored their reversals and the glided distances between reversals. Filaments within the preferred microenvironment glided distances shorter than their own length between reversals that anchored them in their position as a microbial mat. Filaments in the oxic region above the mat or in the sulfidic, anoxic region below the mat glided distances longer than the filament length between reversals. This reversal behavior resulted in a diffusion-like spreading of the filaments. A numerical model of such gliding filaments was constructed based on our observations. The model was applied to virtual filaments in the oxygen- and sulfide-free zone of the sediment, which is a main habitat of Beggiatoa in the natural environment. The model predicts a long residence time of the virtual filament in the suboxic zone and explains why Beggiatoa accumulate high nitrate concentrations in internal vacuoles as an alternative electron acceptor to oxygen.
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filamentous sulfur bacteria Beggiatoa spp in arctic marine sediments svalbard 79 n
FEMS Microbiology Ecology, 2010Co-Authors: Bo Barker Jorgensen, Rita Dunker, Stefanie Grünke, Hans RøyAbstract:Fjord sediments on the west coast of the arctic archipelago Svalbard were surveyed to understand whether large filamentous sulfur bacteria of the genus Beggiatoa thrive at seawater temperatures permanently near freezing. Two sediments had abundant populations of Beggiatoa, while at six sites, only sporadic occurrences were observed. We conclude that Beggiatoa, although previously unnoticed, are widespread in these arctic fjord sediments. Beggiatoa ranged in diameter from 2 to 52 microm and, by those tested, stored nitrate in vacuoles at up to 260 mM. The 16S rRNA gene sequence of a 20-microm-wide filament is closely associated with other large, marine, nitrate-storing Beggiatoa. The Beggiatoa mostly occurred in the upper 2-5 cm of oxidized surface sediment between oxygen and the deeper sulfidic zone. In spite of a very low or an undetectable sulfide concentration, sulfate reduction provided abundant H(2)S in this zone. The total living biomass of Beggiatoa filaments at one study site varied over 3 years between 1.13 and 3.36 g m(-2). Because of their large size, Beggiatoa accounted for up to 15% of the total prokaryotic biomass, even though the filament counts at this site were rather low, comprising <1/10,000 of the bacterial numbers on a cell basis.
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Filamentous sulfur bacteria, Beggiatoa spp., in arctic marine sediments (Svalbard, 79°N)
FEMS microbiology ecology, 2010Co-Authors: Bo Barker Jorgensen, Rita Dunker, Stefanie Grünke, Hans RøyAbstract:Fjord sediments on the west coast of the arctic archipelago Svalbard were surveyed to understand whether large filamentous sulfur bacteria of the genus Beggiatoa thrive at seawater temperatures permanently near freezing. Two sediments had abundant populations of Beggiatoa, while at six sites, only sporadic occurrences were observed. We conclude that Beggiatoa, although previously unnoticed, are widespread in these arctic fjord sediments. Beggiatoa ranged in diameter from 2 to 52 microm and, by those tested, stored nitrate in vacuoles at up to 260 mM. The 16S rRNA gene sequence of a 20-microm-wide filament is closely associated with other large, marine, nitrate-storing Beggiatoa. The Beggiatoa mostly occurred in the upper 2-5 cm of oxidized surface sediment between oxygen and the deeper sulfidic zone. In spite of a very low or an undetectable sulfide concentration, sulfate reduction provided abundant H(2)S in this zone. The total living biomass of Beggiatoa filaments at one study site varied over 3 years between 1.13 and 3.36 g m(-2). Because of their large size, Beggiatoa accounted for up to 15% of the total prokaryotic biomass, even though the filament counts at this site were rather low, comprising
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Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
PLoS biology, 2007Co-Authors: Marc Mußmann, Bo Barker Jorgensen, Dirk De Beer, Rudolf Amann, Michael Richter, André Preisler, Marcel Huntemann, Frank Oliver Glöckner, Werner J.h. KoopmanAbstract:Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments.
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biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment
The ISME Journal, 2007Co-Authors: André Preisler, Dirk De Beer, Antje Boetius, Anna Lichtschlag, Gaute Lavik, Bo Barker JorgensenAbstract:The ecological niche of nitrate-storing Beggiatoa, and their contribution to the removal of sulfide were investigated in coastal sediment. With microsensors a clear suboxic zone of 2-10 cm thick was identified, where neither oxygen nor free sulfide was detectable. In this zone most of the Beggiatoa were found, where they oxidize sulfide with internally stored nitrate. The sulfide input into the suboxic zone was dominated by an upward sulfide flux from deeper sediment, whereas the local production in the suboxic zone was much smaller. Despite their abundance, the calculated sulfide-oxidizing capacity of the Beggiatoa could account for only a small fraction of the total sulfide removal in the sediment. Consequently, most of the sulfide flux into the suboxic layer must have been removed by chemical processes, mainly by precipitation with Fe2+ and oxidation by Fe(III), which was coupled with a pH increase. The free Fe2+ diffusing upwards was oxidized by Mn(IV), resulting in a strong pH decrease. The nitrate storage capacity allows Beggiatoa to migrate randomly up and down in anoxic sediments with an accumulated gliding distance of 4 m before running out of nitrate. We propose that the steep sulfide gradient and corresponding high sulfide flux, a typical characteristic of Beggiatoa habitats, is not needed for their metabolic performance, but rather used as a chemotactic cue by the highly motile filaments to avoid getting lost at depth in the sediment. Indeed sulfide is a repellent for Beggiatoa.
Heide N. Schulz-vogt - One of the best experts on this subject based on the ideXlab platform.
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Simultaneous Visualization of Enzymatic Activity in the Cytoplasm and at Polyphosphate Inclusions in Beggiatoa sp. Strain 35Flor Incubated with 18O-Labeled Water.
mSphere, 2018Co-Authors: Simon Langer, Angela Vogts, Heide N. Schulz-vogtAbstract:ABSTRACT Here we report on a new nanoscale secondary ion mass spectrometry (nanoSIMS) approach based on enzyme-mediated oxygen isotope exchange, which combines the visualization of general metabolic activity in the cytoplasm with insights into the activity of enzymes related to polyphosphate (polyP) inclusions. The polyP-accumulating strain of the large sulfur bacterium Beggiatoa was used as a model organism. Beggiatoa cultures were grown under oxic and anoxic conditions when exposed to either low- or high-sulfide conditions, which are known to influence polyP metabolism in this strain. Subsequent incubation with 18O-labeled water led to high 18O enrichments above the natural background in the cytoplasm and polyP granules derived from enzymatically mediated oxygen isotope exchange. The relative importance of polyP under the different sulfide regimes became evident by an apparent continued metabolic activity at polyP inclusions under stressfully high sulfide concentrations, in contrast to a decreased general metabolic activity in the cytoplasm. This finding confirms the role of polyP as a critical component in bacterial stress response and maintenance of a survival metabolism. IMPORTANCE Microbial organisms exert a large influence on the environment as they directly affect the turnover of essential elements. This is particularly true for polyphosphate-accumulating large sulfur bacteria, which can either accumulate phosphate as polyphosphate or degrade it and release phosphate into the environment, depending on environmental conditions. This study presents a new approach to simultaneously visualize general metabolic activity and enzymatic activity at polyphosphate granules by incubation with 18O-labeled water as the only stable isotope tracer. For this purpose, the well-studied Beggiatoa sp. strain 35Flor was used as a model organism and was exposed to different stress regimes. General metabolic activity was strongly impaired during high-stress regimes. In contrast, intense intracellular polyP cycling was not restricted to favorable or stressful conditions, highlighting the importance of polyP for general cell physiology, especially during hostile conditions. The nanoSIMS approach adds a new tool to study microorganisms involved in phosphorus cycling in the environment together with the identification of general metabolic activity.
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Simultaneous Visualization of Enzymatic Activity in the Cytoplasm and at Polyphosphate Inclusions in Beggiatoa sp. Strain 35Flor Incubated with 18O-Labeled Water
American Society for Microbiology, 2018Co-Authors: Simon Langer, Angela Vogts, Heide N. Schulz-vogtAbstract:Microbial organisms exert a large influence on the environment as they directly affect the turnover of essential elements. This is particularly true for polyphosphate-accumulating large sulfur bacteria, which can either accumulate phosphate as polyphosphate or degrade it and release phosphate into the environment, depending on environmental conditions. This study presents a new approach to simultaneously visualize general metabolic activity and enzymatic activity at polyphosphate granules by incubation with 18O-labeled water as the only stable isotope tracer. For this purpose, the well-studied Beggiatoa sp. strain 35Flor was used as a model organism and was exposed to different stress regimes. General metabolic activity was strongly impaired during high-stress regimes. In contrast, intense intracellular polyP cycling was not restricted to favorable or stressful conditions, highlighting the importance of polyP for general cell physiology, especially during hostile conditions. The nanoSIMS approach adds a new tool to study microorganisms involved in phosphorus cycling in the environment together with the identification of general metabolic activity.Here we report on a new nanoscale secondary ion mass spectrometry (nanoSIMS) approach based on enzyme-mediated oxygen isotope exchange, which combines the visualization of general metabolic activity in the cytoplasm with insights into the activity of enzymes related to polyphosphate (polyP) inclusions. The polyP-accumulating strain of the large sulfur bacterium Beggiatoa was used as a model organism. Beggiatoa cultures were grown under oxic and anoxic conditions when exposed to either low- or high-sulfide conditions, which are known to influence polyP metabolism in this strain. Subsequent incubation with 18O-labeled water led to high 18O enrichments above the natural background in the cytoplasm and polyP granules derived from enzymatically mediated oxygen isotope exchange. The relative importance of polyP under the different sulfide regimes became evident by an apparent continued metabolic activity at polyP inclusions under stressfully high sulfide concentrations, in contrast to a decreased general metabolic activity in the cytoplasm. This finding confirms the role of polyP as a critical component in bacterial stress response and maintenance of a survival metabolism
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Oxidation of Molecular Hydrogen by a Chemolithoautotrophic Beggiatoa Strain
Applied and environmental microbiology, 2016Co-Authors: Annechristin Kreutzmann, Heide N. Schulz-vogtAbstract:ABSTRACT 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. 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.
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Sulfur Respiration in a Marine Chemolithoautotrophic Beggiatoa Strain
Frontiers in microbiology, 2012Co-Authors: Anne Schwedt, Annechristin Kreutzmann, Lubos Polerecky, Heide N. Schulz-vogtAbstract:The chemolithoautotrophic strain Beggiatoa sp. 35Flor shows an unusual migration behavior when cultivated in a gradient medium under high sulfide fluxes. As common for Beggiatoa spp., the filaments form a mat at the oxygen-sulfide interface. However, upon prolonged incubation, a subpopulation migrates actively downwards into the anoxic and sulfidic section of the medium, where the filaments become gradually depleted in their sulfur and polyhydroxyalkanoates (PHA) inclusions. This depletion is correlated with the production of hydrogen sulfide. The sulfur- and PHA-depleted filaments return to the oxygen-sulfide interface, where they switch back to depositing sulfur and PHA by aerobic sulfide oxidation. Based on these observations we conclude that internally stored elemental sulfur is respired at the expense of stored PHA under anoxic conditions. Until now, nitrate has always been assumed to be the alternative electron acceptor in chemolithoautotrophic Beggiatoa spp. under anoxic conditions. As the medium and the filaments were free of oxidized nitrogen compounds we can exclude this metabolism. Furthermore, sulfur respiration with PHA under anoxic conditions has so far only been described for heterotrophic Beggiatoa spp., but our medium did not contain accessible organic carbon. Hence the PHA inclusions must originate from atmospheric CO2 fixed by the filaments while at the oxygen-sulfide interface. We propose that the directed migration of filaments into the anoxic section of an oxygen-sulfide gradient system is used as a last resort to preserve cell integrity, which would otherwise be compromised by excessive sulfur deposition occurring in the presence of oxygen and high sulfide fluxes. The regulating mechanism of this migration is still unknown.
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Unusual polyphosphate inclusions observed in a marine Beggiatoa strain
Antonie van Leeuwenhoek, 2011Co-Authors: Jörg Brock, Erhard Rhiel, Martin Beutler, Verena Salman, Heide N. Schulz-vogtAbstract:Sulfide-oxidizing bacteria of the genus Beggiatoa are known to accumulate phosphate intracellularly as polyphosphate but little is known about the structure and properties of these inclusions. Application of different staining techniques revealed the presence of unusually large polyphosphate inclusions in the marine Beggiatoa strain 35Flor. The inclusions showed a co-occurrence of polyphosphate, calcium and magnesium when analyzed by scanning electron microscopy and energy dispersive X-ray analysis. Similar to polyphosphate-enriched acidocalcisomes of prokaryotes and eukaryotes, the polyphosphate inclusions in Beggiatoa strain 35Flor are enclosed by a lipid layer and store cations. However, they are not notably acidic. 16S rRNA gene sequence-based phylogenetic reconstruction showed an affiliation of Beggiatoa strain 35Flor to a monophyletic branch, comprising other narrow vacuolated and non-vacuolated Beggiatoa species. The polyphosphate inclusions represent a new type of membrane surrounded storage compartment within the genus Beggiatoa, distinct from the mostly nitrate-storing vacuoles known from other marine sulfide-oxidizing bacteria of the family Beggiatoaceae.
Antje Boetius - One of the best experts on this subject based on the ideXlab platform.
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geochemical processes and chemosynthetic primary production in different thiotrophic mats of the hakon mosby mud volcano barents sea
Limnology and Oceanography, 2010Co-Authors: Anna Lichtschlag, Antje Boetius, Janine Felden, Volker Bruchert, Dirk De BeerAbstract:We have investigated if in a cold seep methane or sulfide is used for chemosynthetic primary production and if significant amounts of the sulfide produced by anaerobic oxidation of methane are oxidized geochemically and hence are not available for chemosynthetic production. Geochemically controlled redox reactions and biological turnover were compared in different habitats of the Ha°kon Mosby Mud Volcano. The center of the mud volcano is characterized by the highest fluid flow, and most primary production by the microbial community depends on oxidation of methane. The small amount of sulfide produced is oxidized geochemically with oxygen or is precipitated with dissolved iron. In the medium flow peripheral Beggiatoa habitat sulfide is largely oxidized biologically. The oxygen and nitrate supply is high enough that Beggiatoa can oxidize the sulfide completely, and chemical sulfide oxidation or precipitation is not important. An internally stored nitrate reservoir with average concentrations of 110 mmol L21 enables the Beggiatoa to oxidize sulfide anaerobically. The pH profile indicates sequential sulfide oxidation with elemental sulfur as an intermediate. Gray thiotrophic mats associated with perturbed sediments showed a high heterogeneity in sulfate turnover and high sulfide fluxes, balanced by the opposing oxygen and nitrate fluxes so that biological oxidation dominates over geochemical sulfide removal processes. The three habitats indicate substantial small-scale variability in carbon fixation pathways, either through direct biological use of methane or through indirect carbon fixation of methane-derived carbon dioxide by chemolithotrophic sulfide oxidation.
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biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment
The ISME Journal, 2007Co-Authors: André Preisler, Dirk De Beer, Antje Boetius, Anna Lichtschlag, Gaute Lavik, Bo Barker JorgensenAbstract:The ecological niche of nitrate-storing Beggiatoa, and their contribution to the removal of sulfide were investigated in coastal sediment. With microsensors a clear suboxic zone of 2-10 cm thick was identified, where neither oxygen nor free sulfide was detectable. In this zone most of the Beggiatoa were found, where they oxidize sulfide with internally stored nitrate. The sulfide input into the suboxic zone was dominated by an upward sulfide flux from deeper sediment, whereas the local production in the suboxic zone was much smaller. Despite their abundance, the calculated sulfide-oxidizing capacity of the Beggiatoa could account for only a small fraction of the total sulfide removal in the sediment. Consequently, most of the sulfide flux into the suboxic layer must have been removed by chemical processes, mainly by precipitation with Fe2+ and oxidation by Fe(III), which was coupled with a pH increase. The free Fe2+ diffusing upwards was oxidized by Mn(IV), resulting in a strong pH decrease. The nitrate storage capacity allows Beggiatoa to migrate randomly up and down in anoxic sediments with an accumulated gliding distance of 4 m before running out of nitrate. We propose that the steep sulfide gradient and corresponding high sulfide flux, a typical characteristic of Beggiatoa habitats, is not needed for their metabolic performance, but rather used as a chemotactic cue by the highly motile filaments to avoid getting lost at depth in the sediment. Indeed sulfide is a repellent for Beggiatoa.
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in situ fluxes and zonation of microbial activity in surface sediments of the hakon mosby mud volcano
Limnology and Oceanography, 2006Co-Authors: Dirk De Beer, Eberhard Sauter, Helge Niemann, Norbert Kaul, J P Foucher, Ursula Witte, Michael Schluter, Antje BoetiusAbstract:From the Hakon Mosby Mud Volcano (HMMV) on the southwest Barents Sea shelf, gas and fluids are expelled by active mud volcanism. We studied the mass transfer phenomena and microbial conversions in the surface layers using in situ microsensor measurements and on retrieved cores. The HMMV consists of three concentric habitats: a central area with gray mud, a surrounding area covered by white mats of big sulfide oxidizing filamentous bacteria (Beggiatoa), and a peripheral area colonized by symbiontic tube worms (Pogonophora). A fourth habitat comprised gray microbial mats near gas seeps. The differences between these four methane-fueled habitats are best explained by different transport rates of sulfate into the sediments and pore- water upflow rates. The upflow velocities were estimated by two independent methods at 3-6 m yr21 in the central area and 0.3-1 m yr21 in Beggiatoa mats. In the central area no sulfide was found, indicating that the rapidly rising sulfate-free fluids caused sulfate limitation that inhibited anaerobic oxidation of methane (AOM). Under Beggiatoa mats a steep sulfide peak was found at 2 to 3 cm below the seafloor (bsf), most likely due to AOM. All sulfide was oxidized anaerobically, possibly through nitrate reduction by Beggiatoa. The Beggiatoa mats were dominated by a single filamentous morphotype with a diameter of 10 mm and abundant sulfur inclusions. A high diversity of sulfide oxidizer morphotypes was observed in a grayish microbial mat near gas vents, where aerobic sulfide oxidation was important. The sediments colonized by Pogonophora were influenced by bioventilation, allowing sulfate penetration and AOM to 70 cm bsf. The HMMV is a unique and diverse ecosystem, the structure and functioning of which is mainly controlled by pore-water flow.
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the anaerobic oxidation of methane and sulfate reduction in sediments from gulf of mexico cold seeps
Chemical Geology, 2004Co-Authors: Samantha B. Joye, Heide N. Schulz, Antje Boetius, Beth N Orcutt, Joseph P Montoya, Matthew J Erickson, Samantha K LugoAbstract:We determined the geochemical characteristics of sediments and measured rates of the anaerobic oxidation of methane (AOM) and sulfate reduction (SR) in samples collected near thermogenic (structure II) gas hydrate mounds and in areas lacking hydrates along the continental slope in the Gulf of Mexico. We used radiotracer (C-14 and S-35) techniques to determine rates of AOM and SR over depth in sediment cores. Abundant mats of white and orange Beggiatoa spp. were common in areas of active seepage and these sediments were enriched in hydrogen sulfide and methane. In cores collected from areas without Beggiatoa or hydrate, concentrations of redox metabolites showed little variation over depth and these sites were inferred to be areas of low seepage. Integrated AOM rates were low in Beggiatoa-free cores (<0.05 mmol m−2 day−1) and averaged 2.8±4.6 mmol m−2 day−1 in seep cores that contained Beggiatoa or gas hydrate. Integrated SR rates were also low in Beggiatoa-free cores (<1 mmol m−2 day−1) and averaged 54±94 mmol m−2 day−1 in cores with Beggiatoa or hydrate. Rates of SR generally exceeded rates of AOM and the two processes were loosely coupled, suggesting that the majority of SR at Gulf of Mexico hydrocarbon seep sites is likely fueled by the oxidation of other organic matter, possibly other hydrocarbons and oil, rather than by AOM.
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The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps
Chemical Geology, 2004Co-Authors: Samantha B. Joye, Heide N. Schulz, Antje Boetius, Beth N Orcutt, Joseph P Montoya, Matthew J Erickson, Samantha K LugoAbstract:We determined the geochemical characteristics of sediments and measured rates of the anaerobic oxidation of methane (AOM) and sulfate reduction (SR) in samples collected near thermogenic (structure II) gas hydrate mounds and in areas lacking hydrates along the continental slope in the Gulf of Mexico. We used radiotracer (C-14 and S-35) techniques to determine rates of AOM and SR over depth in sediment cores. Abundant mats of white and orange Beggiatoa spp. were common in areas of active seepage and these sediments were enriched in hydrogen sulfide and methane. In cores collected from areas without Beggiatoa or hydrate, concentrations of redox metabolites showed little variation over depth and these sites were inferred to be areas of low seepage. Integrated AOM rates were low in Beggiatoa-free cores (
Dirk De Beer - One of the best experts on this subject based on the ideXlab platform.
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Close association of active nitrifiers with Beggiatoa mats covering deep-sea hydrothermal sediments.
Environmental microbiology, 2013Co-Authors: Matthias Winkel, Dirk De Beer, Gaute Lavik, Jörg Peplies, Marc MußmannAbstract:Summary Hydrothermal sediments in the Guaymas Basin are covered by microbial mats that are dominated by nitrate-respiring and sulphide-oxidizing Beggiatoa. The presence of these mats strongly correlates with sulphide- and ammonium-rich fluids venting from the subsurface. Because ammonium and oxygen form opposed gradients at the sediment surface, we hypothesized that nitrification is an active process in these Beggiatoa mats. Using biogeochemical and molecular methods, we measured nitrification and determined the diversity and abundance of nitrifiers. Nitrification rates ranged from 74 to 605 μmol N l−1 mat day−1, which exceeded those previously measured in hydrothermal plumes and other deep-sea habitats. Diversity and abundance analyses of archaeal and bacterial ammonia monooxygenase subunit A genes, archaeal 16S ribosomal RNA pyrotags and fluorescence in situ hybridization confirmed that ammonia- and nitrite-oxidizing microorganisms were associated with Beggiatoa mats. Intriguingly, we observed cells of bacterial and potential thaumarchaeotal ammonia oxidizers attached to narrow, Beggiatoa-like filaments. Such a close spatial coupling of nitrification and nitrate respiration in mats of large sulphur bacteria is novel and may facilitate mat-internal cycling of nitrogen, thereby reducing loss of bioavailable nitrogen in deep-sea sediments.
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Vacuolated Beggiatoa-like filaments from different hypersaline environments form a novel genus
Environmental microbiology, 2011Co-Authors: Susanne Hinck, Dirk De Beer, Verena Salman, Marc Mußmann, Thomas R. Neu, Sabine Lenk, Henk M. JonkersAbstract:Summary In this study, members of a specific group of thin (6–14 µm filament diameter), vacuolated Beggiatoa-like filaments from six different hypersaline microbial mats were morphologically and phylogenetically characterized. Therefore, enrichment cultures were established, filaments were stained with fluorochromes to show intracellular structures and 16S rRNA genes were sequenced. Morphological characteristics of Beggiatoa-like filaments, in particular the presence of intracellular vacuoles, and the distribution of nucleic acids were visualized. In the intracellular vacuole nitrate reached concentrations of up to 650 mM. Fifteen of the retrieved 16S rRNA gene sequences formed a monophyletic cluster and were phylogenetically closely related (≥ 94.4% sequence identity). Sequences of known filamentous sulfide-oxidizing genera Beggiatoa and Thioploca that comprise non-vacuolated and vacuolated filaments from diverse habitats clearly delineated from this cluster. The novel monophyletic cluster was furthermore divided into two sub-clusters: one contained sequences originating from Guerrero Negro (Mexico) microbial mats and the other comprised sequences from five distinct Spanish hypersaline microbial mats from Ibiza, Formentera and Lake Chiprana. Our data suggest that Beggiatoa-like filaments from hypersaline environments displaying a thin filament diameter contain nitrate-storing vacuoles and are phylogenetically separate from known Beggiatoa. Therefore, we propose a novel genus for these organisms, which we suggest to name ‘Candidatus AlloBeggiatoa’.
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geochemical processes and chemosynthetic primary production in different thiotrophic mats of the hakon mosby mud volcano barents sea
Limnology and Oceanography, 2010Co-Authors: Anna Lichtschlag, Antje Boetius, Janine Felden, Volker Bruchert, Dirk De BeerAbstract:We have investigated if in a cold seep methane or sulfide is used for chemosynthetic primary production and if significant amounts of the sulfide produced by anaerobic oxidation of methane are oxidized geochemically and hence are not available for chemosynthetic production. Geochemically controlled redox reactions and biological turnover were compared in different habitats of the Ha°kon Mosby Mud Volcano. The center of the mud volcano is characterized by the highest fluid flow, and most primary production by the microbial community depends on oxidation of methane. The small amount of sulfide produced is oxidized geochemically with oxygen or is precipitated with dissolved iron. In the medium flow peripheral Beggiatoa habitat sulfide is largely oxidized biologically. The oxygen and nitrate supply is high enough that Beggiatoa can oxidize the sulfide completely, and chemical sulfide oxidation or precipitation is not important. An internally stored nitrate reservoir with average concentrations of 110 mmol L21 enables the Beggiatoa to oxidize sulfide anaerobically. The pH profile indicates sequential sulfide oxidation with elemental sulfur as an intermediate. Gray thiotrophic mats associated with perturbed sediments showed a high heterogeneity in sulfate turnover and high sulfide fluxes, balanced by the opposing oxygen and nitrate fluxes so that biological oxidation dominates over geochemical sulfide removal processes. The three habitats indicate substantial small-scale variability in carbon fixation pathways, either through direct biological use of methane or through indirect carbon fixation of methane-derived carbon dioxide by chemolithotrophic sulfide oxidation.
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Physiological adaptation of a nitrate-storing Beggiatoa sp. to diel cycling in a phototrophic hypersaline mat.
Applied and environmental microbiology, 2007Co-Authors: Susanne Hinck, Dirk De Beer, Marc Mußmann, Gaute Lavik, Thomas R. Neu, Henk M. JonkersAbstract:The aim of this study was to investigate the supposed vertical diel migration and the accompanying physiology of Beggiatoa bacteria from hypersaline microbial mats. We combined microsensor, stable-isotope, and molecular techniques to clarify the phylogeny and physiology of the most dominant species inhabiting mats of the natural hypersaline Lake Chiprana, Spain. The most dominant morphotype had a filament diameter of 6 to 8 μm and a length varying from 1 to >10 mm. Phylogenetic analysis by 16S rRNA gene comparison revealed that this type appeared to be most closely related (91% sequence identity) to the narrow (4-μm diameter) nonvacuolated marine strain MS-81-6. Stable-isotope analysis showed that the Lake Chiprana species could store nitrate intracellularly to 40 mM. The presence of large intracellular vacuoles was confirmed by fluorescein isothiocyanate staining and subsequent confocal microscopy. In illuminated mats, their highest abundance was found at a depth of 8 mm, where oxygen and sulfide co-occurred. However, in the dark, the highest Beggiatoa densities occurred at 7 mm, and the whole population was present in the anoxic zone of the mat. Our findings suggest that hypersaline Beggiatoa bacteria oxidize sulfide with oxygen under light conditions and with internally stored nitrate under dark conditions. It was concluded that nitrate storage by Beggiatoa is an optimal strategy to both occupy the suboxic zones in sulfidic sediments and survive the dark periods in phototrophic mats.
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Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
PLoS biology, 2007Co-Authors: Marc Mußmann, Bo Barker Jorgensen, Dirk De Beer, Rudolf Amann, Michael Richter, André Preisler, Marcel Huntemann, Frank Oliver Glöckner, Werner J.h. KoopmanAbstract:Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments.
Hans Røy - One of the best experts on this subject based on the ideXlab platform.
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Motility patterns of filamentous sulfur bacteria, Beggiatoa spp.
FEMS microbiology ecology, 2011Co-Authors: Rita Dunker, Anja Kamp, Hans Røy, Bo Barker JorgensenAbstract:The large sulfur bacteria, Beggiatoa spp., live on the oxidation of sulfide with oxygen or nitrate, but avoid high concentrations of both sulfide and oxygen. As gliding filaments, they rely on reversals in the gliding direction to find their preferred environment, the oxygen–sulfide interface. We observed the chemotactic patterns of single filaments in a transparent agar medium and scored their reversals and the glided distances between reversals. Filaments within the preferred microenvironment glided distances shorter than their own length between reversals that anchored them in their position as a microbial mat. Filaments in the oxic region above the mat or in the sulfidic, anoxic region below the mat glided distances longer than the filament length between reversals. This reversal behavior resulted in a diffusion-like spreading of the filaments. A numerical model of such gliding filaments was constructed based on our observations. The model was applied to virtual filaments in the oxygen- and sulfide-free zone of the sediment, which is a main habitat of Beggiatoa in the natural environment. The model predicts a long residence time of the virtual filament in the suboxic zone and explains why Beggiatoa accumulate high nitrate concentrations in internal vacuoles as an alternative electron acceptor to oxygen.
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filamentous sulfur bacteria Beggiatoa spp in arctic marine sediments svalbard 79 n
FEMS Microbiology Ecology, 2010Co-Authors: Bo Barker Jorgensen, Rita Dunker, Stefanie Grünke, Hans RøyAbstract:Fjord sediments on the west coast of the arctic archipelago Svalbard were surveyed to understand whether large filamentous sulfur bacteria of the genus Beggiatoa thrive at seawater temperatures permanently near freezing. Two sediments had abundant populations of Beggiatoa, while at six sites, only sporadic occurrences were observed. We conclude that Beggiatoa, although previously unnoticed, are widespread in these arctic fjord sediments. Beggiatoa ranged in diameter from 2 to 52 microm and, by those tested, stored nitrate in vacuoles at up to 260 mM. The 16S rRNA gene sequence of a 20-microm-wide filament is closely associated with other large, marine, nitrate-storing Beggiatoa. The Beggiatoa mostly occurred in the upper 2-5 cm of oxidized surface sediment between oxygen and the deeper sulfidic zone. In spite of a very low or an undetectable sulfide concentration, sulfate reduction provided abundant H(2)S in this zone. The total living biomass of Beggiatoa filaments at one study site varied over 3 years between 1.13 and 3.36 g m(-2). Because of their large size, Beggiatoa accounted for up to 15% of the total prokaryotic biomass, even though the filament counts at this site were rather low, comprising <1/10,000 of the bacterial numbers on a cell basis.
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Filamentous sulfur bacteria, Beggiatoa spp., in arctic marine sediments (Svalbard, 79°N)
FEMS microbiology ecology, 2010Co-Authors: Bo Barker Jorgensen, Rita Dunker, Stefanie Grünke, Hans RøyAbstract:Fjord sediments on the west coast of the arctic archipelago Svalbard were surveyed to understand whether large filamentous sulfur bacteria of the genus Beggiatoa thrive at seawater temperatures permanently near freezing. Two sediments had abundant populations of Beggiatoa, while at six sites, only sporadic occurrences were observed. We conclude that Beggiatoa, although previously unnoticed, are widespread in these arctic fjord sediments. Beggiatoa ranged in diameter from 2 to 52 microm and, by those tested, stored nitrate in vacuoles at up to 260 mM. The 16S rRNA gene sequence of a 20-microm-wide filament is closely associated with other large, marine, nitrate-storing Beggiatoa. The Beggiatoa mostly occurred in the upper 2-5 cm of oxidized surface sediment between oxygen and the deeper sulfidic zone. In spite of a very low or an undetectable sulfide concentration, sulfate reduction provided abundant H(2)S in this zone. The total living biomass of Beggiatoa filaments at one study site varied over 3 years between 1.13 and 3.36 g m(-2). Because of their large size, Beggiatoa accounted for up to 15% of the total prokaryotic biomass, even though the filament counts at this site were rather low, comprising
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Video-supported Analysis of Beggiatoa Filament Growth, Breakage, and Movement
Microbial ecology, 2008Co-Authors: Anja Kamp, Hans Røy, Heide N. Schulz-vogtAbstract:A marine Beggiatoa sp. was cultured in semi-solid agar with opposing oxygen-sulfide gradients. Growth pattern, breakage of filaments for multiplication, and movement directions of Beggiatoa filaments in the transparent agar were investigated by time-lapse video recording. The initial doubling time of cells was 15.7 ± 1.3 h (mean ± SD) at room temperature. Filaments grew up to an average length of 1.7 ± 0.2 mm, but filaments of up to approximately 6 mm were also present. First breakages of filaments occurred approximately 19 h after inoculation, and time-lapse movies illustrated that a parent filament could break into several daughter filaments within a few hours. In >20% of the cases, filament breakage occurred at the tip of a former loop. As filament breakage is accomplished by the presence of sacrificial cells, loop formation and the presence of sacrificial cells must coincide. We hypothesize that sacrificial cells enhance the chance of loop formation by interrupting the communication between two parts of one filament. With communication interrupted, these two parts of one filament can randomly move toward each other forming the tip of a loop at the sacrificial cell.