Dense Populations of a Giant Sulfur Bacterium in Namibian Shelf Sediments

Schulz, Heide N.; Brinkhoff, Thorsten; Ferdelman, Timothy G.; Mariné, M. Hernández; Teske, Andreas; Jørgensen, Bo Barker

doi:10.1126/science.284.5413.493

Cited by 449 publications

(391 citation statements)

References 16 publications

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“…The volume of their large cells is mostly occupied by vacuoles, which serve as nitrate reservoirs. The accumulated nitrate enables them to oxidize reduced sulfur compounds even in the absence of external electron acceptors (7,21,28).…”

Section: Introductionmentioning

confidence: 99%

“…All known nitrate-storing sulfur oxidizers belong to a particular phylogenetic cluster (1,14,28,31). At the present time, they are classified into three genera based on their morphological traits.…”

Section: Introductionmentioning

confidence: 99%

“…At the present time, they are classified into three genera based on their morphological traits. The bacterium with the largest cell volume belongs to the genus Thiomargarita, and its appearance can be described as a chain of spherical cells (28). Bacteria of the other two genera, Beggiatoa and Thioploca are filamentous.…”

Section: Introductionmentioning

confidence: 99%

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Community Structure of Bacteria Associated with Sheaths of Freshwater and Brackish Thioploca Species

2006

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Bacterial communities associated with sheaths of Thioploca spp. from two freshwater lakes (Lake Biwa, Japan, and Lake Constance, Germany) and one brackish lake (Lake Ogawara, Japan) were analyzed with denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene fragments. The comparison between the DGGE band patterns of bulk sediment and Thioploca filaments of Lake Biwa suggested the presence of specific bacterial communities associated with Thioploca sheaths. As members of sheath-associated communities, bacteria belonging to Bacteroidetes were detected from the samples of both freshwater lakes. A DGGE band from Thioploca of Lake Biwa, belonging to candidate division OP8, was quite closely related to another DGGE band detected from that of Lake Constance. In contrast to the case of freshwater lakes, no bacterium of Bacteroidetes or OP8 was detected from Thioploca of Lake Ogawara.However, two DGGE bands from Lake Ogawara, belonging to Chloroflexi, were quite closely related to a DGGE band from Lake Constance. Two DGGE bands obtained from Lake Biwa were closely related to phylogenetically distant dissimilatory

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Community Structure of Bacteria Associated with Sheaths of Freshwater and Brackish Thioploca Species

2006

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“…A third species, Achromatium volutans, is not phylogenetically characterized, and was described as marine sulfur-containing cells without calcite (Hinze, 1903;Nadson, 1913Nadson, , 1914Kolkwitz, 1918;Skuja, 1948;Van Niel, 1948). Cells matching this morphology were recently phylogenetically classified as members of the Beggiatoaceae (Schulz et al, 1999;Salman et al, 2011Salman et al, , 2013, leading to the family Achromatiaceae now exclusively containing members that deposit intracellular calcite (Gray and Head, 2014).…”

Section: Introductionmentioning

confidence: 99%

Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh

et al. 2015

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Large sulfur bacteria of the genus Achromatium are exceptional among Bacteria and Archaea as they can accumulate high amounts of internal calcite. Although known for more than 100 years, they remain uncultured, and only freshwater populations have been studied so far. Here we investigate a marine population of calcite-accumulating bacteria that is primarily found at the sediment surface of tide pools in a salt marsh, where high sulfide concentrations meet oversaturated oxygen concentrations during the day. Dynamic sulfur cycling by phototrophic sulfide-oxidizing and heterotrophic sulfate-reducing bacteria co-occurring in these sediments creates a highly sulfidic environment that we propose induces behavioral differences in the Achromatium population compared with reported migration patterns in a low-sulfide environment. Fluctuating intracellular calcium/sulfur ratios at different depths and times of day indicate a biochemical reaction of the salt marsh Achromatium to diurnal changes in sedimentary redox conditions. We correlate this calcite dynamic with new evidence regarding its formation/mobilization and suggest general implications as well as a possible biological function of calcite accumulation in large bacteria in the sediment environment that is governed by gradients. Finally, we propose a new taxonomic classification of the salt marsh Achromatium based on their adaptation to a significantly different habitat than their freshwater relatives, as indicated by their differential behavior as well as phylogenetic distance on 16S ribosomal RNA gene level. In future studies, whole-genome characterization and additional ecophysiological factors could further support the distinctive position of salt marsh Achromatium.

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“…Several studies have shown that all these giant sulphur bacteria employ similar metabolic strategies. These include nitrate and sulphur accumulation, mixotrophic assimilation of CO 2 and organic substrates such as acetate, and the ability to perform dissimilatory nitrate reduction to ammonium (DNRA; Fossing et al, 1995;McHatton et al, 1996;Otte et al, 1999;Schulz et al,1999;Sayama et al, 2005). Recent genomic studies of Beggiatoa and physiological studies of Thiomargarita (Schulz and de Beer 2002;Schulz and Schulz 2005;Mussman et al, 2007) indicate that the giant sulphur bacteria have diverse pathways of energy metabolism, which includes both DNRA and denitrification, oxygen respiration and an auxiliary energy reservoir of polyphosphate.…”

Section: Introductionmentioning

confidence: 99%

Physiology and behaviour of marine Thioploca

et al. 2009

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Among prokaryotes, the large vacuolated marine sulphur bacteria are unique in their ability to store, transport and metabolize significant quantities of sulphur, nitrogen, phosphorus and carbon compounds. In this study, unresolved questions of metabolism, storage management and behaviour were addressed in laboratory experiments with Thioploca species collected on the continental shelf off Chile. The Thioploca cells had an aerobic metabolism with a potential oxygen uptake rate of 1760 lmol O 2 per dm 3 biovolume per h, equivalent to 4.4 nmol O 2 per min per mg protein. When high ambient sulphide concentrations (B200 lM) were present, a sulphide uptake of 6220 ± 2230 lmol H 2 S per dm 3 per h, (mean ± s.e.m., n ¼ 4) was measured. This sulphide uptake rate was six times higher than the oxidation rate of elemental sulphur by oxygen or nitrate, thus indicating a rapid sulphur accumulation by Thioploca. Thioploca reduce nitrate to ammonium and we found that dinitrogen was not produced, neither through denitrification nor through anammox activity. Unexpectedly, polyphosphate storage was not detectable by microautoradiography in physiological assays or by staining and microscopy. Carbon dioxide fixation increased when nitrate and nitrite were externally available and when organic carbon was added to incubations. Sulphide addition did not increase carbon dioxide fixation, indicating that Thioploca use excess of sulphide to rapidly accumulate sulphur rather than to accelerate growth. This is interpreted as an adaptation to infrequent high sulphate reduction rates in the seabed. The physiology and behaviour of Thioploca are summarized and the adaptations to an environment, dominated by infrequent oxygen availability and periods of high sulphide abundance, are discussed.

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Dense Populations of a Giant Sulfur Bacterium in Namibian Shelf Sediments

Cited by 449 publications

References 16 publications

Community Structure of Bacteria Associated with Sheaths of Freshwater and Brackish Thioploca Species

Community Structure of Bacteria Associated with Sheaths of Freshwater and Brackish Thioploca Species

Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh

Physiology and behaviour of marine Thioploca

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