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Thioploca spp.: filamentous sulfur bacteria with nitrate vacuoles

Bo Barker Jørgensen, Victor A Gallardo
DOI: http://dx.doi.org/10.1111/j.1574-6941.1999.tb00585.x 301-313 First published online: 1 April 1999


Thioploca spp. are multicellular, filamentous, colorless sulfur bacteria inhabiting freshwater and marine sediments. They have elemental sulfur inclusions similar to the phylogenetically closely related Beggiatoa, but in contrast to these they live in bundles surrounded by a common sheath. Vast communities of large Thioploca species live along the Pacific coast of South America and in other upwelling areas of high organic matter sedimentation with bottom waters poor in oxygen and rich in nitrate. Each cell of these thioplocas harbors a large liquid vacuole which is used as a storage for nitrate with a concentration of up to 500 mM. The nitrate is used as an electron acceptor for sulfide oxidation and the bacteria may grow autotrophically or mixotrophically using acetate or other organic molecules as carbon source. The filaments stretch up into the overlying seawater, from which they take up nitrate, and then glide down 5–15 cm deep into the sediment through their sheaths to oxidize sulfide formed by intensive sulfate reduction. New major occurrences have been found in recent years, both in lakes and in the ocean, and have stimulated the interest in these fascinating bacteria.

  • Thioploca
  • Sulfide-oxidizing bacteria
  • Nitrate respiration
  • Phylogeny of sulfur bacteria
  • Physiology

1 Introduction

The filamentous, colorless sulfur bacteria, Thioploca spp., were first described by the German botanist R. Lauterborn in 1907 [1]. He found bundles of these conspicuous filaments contained in gelatinous sheaths to be abundant in the mud at 15–20 m depth in Lake Constance at the German-Swiss border and he named them according to their appearance: thion for sulfur and ploka for braid. The bacteria had an appearance similar to Beggiatoa arachnoidea: a uniseriate filament with distinct crosswalls, consisting of a row of cylindrical, disk-shaped cells with diameters of 5–9 μm and with many sulfur globules. In contrast to Beggiatoa, the filaments often had tapered ends and occurred as bundles surrounded by a common sheath. When many filaments grew intertwined in a sheath they had the appearance under the microscope of a braid. Lauterborn named the type species Thioploca schmidlei, after his colleague and friend, Prof. W. Schmidle.

Four years later, the Russian microbiologist S.M. Wislouch (Visloukh) found similar but narrower (2–4.5 μm) filaments in sheaths, as he was studying mud samples from the Neva river near St. Petersburg [2]. He described these as a new species, Thioploca ingrica[3], named after the local geographical region, Ingrien. An intensive survey of benthic communities of sulfur bacteria, published by F. Koppe in 1922 [4], showed that thioplocas at that time occurred in several lakes of northern Germany. From Lake Constance he described a third species, Thioploca minima, with only 1–2 μm diameter. He also noted that filaments of different diameters could occur in the same sheath and erroneously gave this supposedly variable species a new name, Thioploca mixta[4,5]. What he had observed was, however, probably a mixture of two species sharing the same sheath. A much later search for thioplocas in Germany by S. Maier and W.C. Preissner in 1976 [6] indicated that these bacteria had disappeared again from many of the old type localities, but new occurrences, e.g. in Lake Erie in the USA, have been found.

New interest in the research on Thioploca arose after the widespread occurrence of very large marine Thioploca species on the Pacific continental shelf of South America was published [7]. These communities had been noticed already many years before by V.A. Gallardo [8] as well as by G.T. Rowe and J. Waterbury, and the slimy material, often trapped in bottom trawls, was known among the local fishermen as estopa (Spanish for uncleansed wool or flax). Their true bacterial origin as giant thioplocas was, however, realized only in 1975 when they were presented to the microbiologist M. Shilo, then visiting Woods Hole.

2 Marine thioplocas

The marine thioplocas discovered in the Pacific were unique in having diameters ranging from 15 to 40 μm and reaching lengths of many cm (Fig. 1). They are thus amongst the largest bacteria known [10]. These marine Thioploca spp. occur in the shelf sediments along the Pacific coast of South America in masses (wet weight including sheath) of up to 1 kg m−2. They have now been reported from many areas of the oxygen minimum zone underlying the Peru-Chile Subsurface Countercurrent system at 40–280 m water depth, a coastline of more than 3000 km and an area exceeding 10 000 km2. This is probably the largest community of visible bacteria in the world.


Marine thioplocas from the shelf off the coast of Chile near Concepción sampled at 50–100 m water depth during summer when the water column over the sea floor was anoxic. A: Sediment core of 8 cm diameter showing the whitish sheaths of thioploca (‘spaghetti bacteria’) extending vertically down from the surface to many cm depth. At the surface a layer of freshly deposited phytodetritus gives the otherwise black sediment a brownish color. B: Thioploca in their transparent sheaths sieved and washed from a sediment sample. The frame is 8 mm wide. C: Thioploca filaments extending up from the sediment surface and into the anoxic but nitrate containing flow of seawater. The frame is 15 mm wide. D: Thioploca araucae filament showing the dense globules of elemental sulfur and the tapered filament end which morphologically often distinguishes Thioploca spp. from Beggiatoa spp. Scale bar is 40 μm. E: Light micrograph of sediment with Thioploca filaments of the two genera, T. chileae (18 μm wide) and T. araucae (35 μm wide). The thin filaments are sulfate reducing bacteria of the genus Desulfonema. An Ω-shaped nematode near the center of the picture shows for comparison the giant size of the thioplocas. F: Bundle of T. araucae extending out of their sheath. The appearence of a braid is seen where the filaments cross over, hence the name Thioploca=sulfur braid. G: Confocal laser scanning micrograph of empty Thioploca sheath covered by filamentous sulfate reducing bacteria, Desulfonema sp. A non-specific fluorescent stain shows how the bacteria are longitudinally oriented on the surface of the sheath. The field is 225 μm wide. H: Transmission electron micrograph of longitudinal thin section of T. chileae in a sheath. The filaments have thin cross-walls and nearly empty cells due to the large liquid vacuoles. In the thin peripheral layer of cytoplasm sulfur globules are stored. The field is 110 μm wide. (Photographs by M. Hüttel (A+B+C+D), B.B. Jørgensen (E+F), T. Neu (G) and S. Maier and H. Voelker (H). Panels B and C are from [9], with permission.)

According to their diameters (Fig. 2), the marine thioplocas fall into several species of which two are considered valid today [11]: the 12–20 μm wide Thioploca chileae and the 30–43 μm wide Thioploca araucae (found near the Gulf of Arauco). A narrower form called Thioploca marina of 2.5–5 μm diameter also occurs commonly on the Chilean shelf, but it is not yet a recognized species. Occasionally, very wide and previously undescribed Thioploca-like filaments of up to 125 μm are found among these communities (H.N. Schulz and B.B. Jørgensen, unpublished observations). This diameter is comparable to the largest Beggiatoa spp. found as thick mats or loose masses around the hydrothermal vents of the Guaymas Basin [12]. Although a taxonomy based on diameters, similar to that used for Beggiatoa spp., is certainly not satisfactory, it appears that the diameters of the Thioploca populations cluster within well defined limits and show less continuity than those of Beggiatoa[13,14](Fig. 2,Table 1).


The diameters of Thioploca filaments are used to define the species. In a sediment sample from 40 m water depth off the Chilean coast, about 250 filament diameters were measured and their relative frequency is shown at ca. 1 μm resolution. Among the filaments living in sheaths (A), the two species, T. chileae and T. araucae, are clearly distinguished, as are the filaments of a narrower species which corresponds to T. marina. The T. marina occurred in larger numbers than indicated. Filaments were also found in large numbers outside sheaths (B). Their size distribution partly differed from that of the thioplocas, which indicated that these were now just thioploca filaments stretching out of their sheaths. As free living filaments, they may be Beggiatoa spp., although the 30–40 μm size class distribution resembles that of the thioplocas. (Data from [13], with permission.)

View this table:

Characteristics of the known types of Thioploca including both valid and non-valid species

NameDiameter (μm)Valid species16S rRNA sequenceReference
Freshwater species
T. minima1–2nono[3]
T. ingrica2–5yesyes[2]
T. schmidlei5–9yesno[1]
Marine species
T. marina2.5–5nono[6]
T. chileae12–20yesyes[11]
T. araucae30–43yesyes[11]
  • The species definition is based on diameters and on freshwater or marine habitat.

2.1 Morphology

The cell lengths of the marine Thioploca spp. are generally 0.5–1.5 times the cell diameter and a single filament may contain more than a thousand cells, thus reaching a total length of up to 7 cm [15]. The cells are separated by septa formed by the cytoplasmic membranes and the innermost layer of the complex, four-layered cell wall [15,16]. Numerous sulfur inclusions are found in the cytoplasm, most probably formed by intrusions of the outer cytoplasmic membrane such as indicated from TEM micrographs of the narrower forms of Beggiatoa and Thioploca[11,15,17]. A unique cellular structure was observed by Maier and coworkers [11,17] by transmission electron microscopy of the large thioplocas. Inside each cell of the filaments they found a central liquid vacuole which filled more than 80% of the total cellular volume and which was bounded by a membrane (Fig. 1H). The active cytoplasm was thus distributed as only a thin layer along the periphery of each cell. Similar large vacuoles were discovered five years later in the giant beggiatoas living around hydrothermal vents [18]. Also the narrow thioplocas appear to have many small, liquid vacuoles enclosed by a triplet membrane of similar appearance as the cytoplasmic membrane [15].

2.2 Physiology

The main energy and carbon metabolism of Thioploca spp. remains uncertain, mainly because no pure culture has yet been obtained of these organisms despite repeated attempts [19]. The Thioploca spp. appear to have a lower tolerance towards oxygen and sulfide than Beggiatoa spp. [19]. This is in accordance with their occurrence in sediments with low sulfide concentration [20], as already noted by Lauterborn in 1907 [1], and in sediments underlying oxygen-depleted water. They have long been expected to be autotrophic or mixotrophic sulfide oxidizers, in analogy with the morphologically very similar Beggiatoa and in accordance with their accumulation of elemental sulfur. The suggestion of Morita and coworkers [21] that the thioplocas off the coast of Chile are methylotrophs, living on methane produced in the sediment and seeping up from coal seams running under the sea floor, appears to be incorrect and due to an overinterpretation of indirect, preliminary data. Thus, the sediments off the Chilean coast, where thioplocas grow densely, have very low production rates and concentrations of methane [20], which could not possibly provide sufficient organic carbon and energy for the large bacterial populations. More careful studies on the potential substrates of the Chilean thioplocas using 14C-labeled substrates combined with autoradiography showed, accordingly, that methane or methanol were not taken up, whereas there was a strong incorporation of acetate, amino acids, bicarbonate, glucose and glycine [22]. The incorporations appeared to be dependent on the presence of sulfide in the medium, which indicates that the thioplocas may be mixotrophic sulfide oxidizers similar to many Beggiatoa strains [23]. Whether they are also able to grow autotrophically like the marine beggiatoas [24], as indicated by their incorporation of H14CO3, still needs to be demonstrated.

2.3 Phylogeny

The filamentous sulfide-oxidizing bacteria Thioploca, Beggiatoa and Thiothrix are considered to be a related group based on their morphology and physiology and are placed together in the family Beggiatoaceae [25]. The phylogenetic relationship was recently tested by 16S rRNA sequence analysis of several Thioploca and Beggiatoa strains [26]. The three Thioploca species studied, T. ingrica, T. chileae and T. araucae, form a monophyletic group within the γ subdivision of the Proteobacteria, closely related to the beggiatoas, whereas Thiothrix followed a different phylogenetic lineage within the gamma-subdivision (Fig. 3). The identification of Thioploca species based on diameters (Fig. 2) was found to provide not only a differentiation of morphotypes but indeed a separation of genospecies. The picture is, however, far from complete and in particular a possible close relationship between the large, vacuolated Thioploca and Beggiatoa species deserves further attention. Preliminary 16S rRNA sequence data indicate that these may be more closely related to each other than the large Beggiatoas are to the small Beggiatoas (A. Teske et al., Syst. Appl. Microbiol., in press). Thus, although the mucus sheaths of Thioploca bundles are very conspicuous, they may reflect only a minor biochemical and behavioral difference from Beggiatoa, which also secrete a fine sheath around individual filaments during their gliding movement. Similarities in morphology and biology between the cyanobacteria, e.g. Oscillatoria or Microcoleus, and the Beggiatoaceae had since the beginning of this century led to the suggestion that the latter were colorless, ‘apochlorotic’ cyanobacteria [2]. The phylogenetic analysis has, however, clearly shown that there is not a close relation between the filamentous, sulfide-oxidizing bacteria and the cyanobacteria, which are not a subdivision of the Proteobacteria, but a separate bacterial phylum.


16S rRNA distance tree of the proteobacterial γ and β subdivisions showing Thioploca, Beggiatoa and representative H2S and sulfur oxidizing bacteria. The species of Thioploca and Beggiatoa are seen to form a phylogenetically coherent group. Sulfate reducing bacteria of the δ subdivision are included as outgroup. The scalebar corresponds to 0.05 substitutions per nucleotide position. Abbreviations: Thb.=Thiobacillus, Ect.=Ectothiorhodospira. (From [26], with permission.)

2.4 Liquid vacuoles

Until recently, the function and the evolutionary niche of the giant filaments and their cells filled with liquid vacuoles was unknown. It was observed by Gundersen and coworkers [27] that the morphologically similar, very large beggiatoas living on the sea floor around hydrothermal vents in the Guaymas Basin built 1–3 cm thick mats with a coarse mesh structure. This, supposedly, had the function of enabling an advective water flow through the mesh without blowing away the beggiatoas, as easily happens with mats of the thinner species [28]. Consequently, the hydrothermal advection could enhance the transport of oxygen and sulfide many-fold over a pure diffusive transport, which has been found to otherwise limit the growth and metabolic rate of mat-forming beggiatoas [29,30]. Larkin and Henk [31], on the other hand, suggested that ‘hollowness’ was an adaptation to the large cell size, whereby diffusive substrate limitation due to an otherwise unfavorable surface-to-volume ratio was alleviated. Although these suggestions are probably both correct, they missed the main secret of these organisms, discovered only years later: the vacuoles function as an electron acceptor reservoir, an ‘anaerobic lung’.

3 Thioploca community on the Chilean shelf

In 1994, a new concerted effort was made to study the Chilean Thioploca communities and their role in the biogeochemical cycles on the South American shelf [32]. Astonishing results came immediately as sediment cores containing Thioploca mats were squeezed to obtain pore water samples for chemical analyses (Fig. 4B). As the pressure was gradually increased, the nitrate concentration measured in the pore water suddenly stepped up from the ambient seawater level of 20–25 μM to 3 mM, i.e. a 100-fold higher concentration [33]. What happened was obviously that the vacuoles of Thioploca burst and released vast amounts of nitrate. Measurements of nitrate concentrations directly in the vacuole fluid were subsequently done by L.P. Nielsen, who cut pieces of a few mm length of individual filaments and extracted the nitrate. The subsequent spectrophotometric analysis revealed extreme concentrations of up to 500 mM NO3[32]. This is equivalent to the molar concentration of chloride in sea water. Elemental sulfur, stored as sulfur globules in the cytoplasm, occurred at a mean concentration of 200–300 μmol cm−3 in the filaments, i.e. in similar amounts as nitrate [20]. A novel picture of the biology of the marine thioplocas emerged from this study, which is summarized in the following sections.


Thioploca distribution and biogeochemistry during summer in the sea floor off the coast of Chile at 90 m water depth. A: Depth distribution of Thioploca in sheaths calculated as ‰ biovolume, i.e. mm3 biovolume per cm3 sediment. B: Depth distribution of free nitrate in the pore water compared to the 100-fold higher pool of nitrate contained in Thioploca vacuoles (sum is ‘total NO3’). The latter was calculated from the Thioploca biovolume multiplied by the mean nitrate concentration in the filaments. Note difference in the two NO3 scales. C: Rates of sulfate reduction in the sediment measured from short-term radiotracer experiments using  35SO2−4. D: Sulfate (○) and sulfide (ΣH2S, ●) in the porewater. (Data from [13,20,33], with permission.)

3.1 Distribution and biomass

In a transect across the Chilean shelf at 36° south, just north of Concepción, thioplocas occurred from about 40 m water depth to beyond the shelf break at 200 m with living biomasses peaking at 120 g wet weight m−2 on the mid-shelf [13]. Although about 90% of Thioploca is liquid vacuoles, the 10% of active biomass, ca. 10 g wet weight m−2, is still comparable to the total biomass of the local benthic fauna [34]. It is also comparable to the biomass of Beggiatoa spp., 5–20 g wet weight m−2, found in marine sediments of the eutrophic Limfjorden [14]. Due to the intense upwelling off the Chilean coast, the overlying sea water is strongly or totally depleted of oxygen with concentrations of <5 μM O2 or <2% air saturation. The thioplocas here build 1–2 cm thick, loose mats in the muddy sea floor, with their dense gelatinous sheaths consolidating the sediment surface, and with 50–500 μm thick strands reaching 10 cm or more down into the sediment (Fig. 1A and Fig. 4A[13]). A three-dimensional mapping of the inhabited sheaths showed that below the mat they form a system of preferentially vertical, unbranched mucus tunnels allowing the gliding filaments to migrate from the surface and deep down into the sediment (Fig. 5).


Three-dimensional reconstruction of Thioploca sheaths in sediment from the Chilean coast at 40 m water depth. The sediment block of 5×2.5×1 cm was rapidly frozen, cut vertically at 100 μm increments with a cryomicrotome, and photographed in polarized light. From 100 sequential photographs, which had been scanned into a computer, the 3-D image was developed. At the sediment surface a grayish color shows a dense mat of free filaments of either Beggiatoa or Thioploca outside their sheaths. Below the mat, dark strands of Thioploca sheaths extended down through the sediment with a mostly vertical orientation. (From [13], with permission.)

The thioplocas appear to move almost continuously with gliding speeds of 1–3 μm s−1, which may enable the bacteria to move 10 cm in a day. The filaments are rather rigid and may stretch several cm up from the sediment surface into the overlying, flowing seawater where they sway back and forth in the boundary layer flow (Fig. 1C). Underwater video recordings from a research submersible on the Peruvian shelf have revealed a ‘white lawn’ of such filaments densely covering the sediment (unpublished observations by M.A. Arthur, W.E. Dean, R. Jahnke and other participants of R/V Seward Johnson cruise SJ-1092). By penetrating the diffusive boundary layer, the thioplocas greatly increase the surface area available for active nitrate uptake. Accordingly, experimental studies have shown that the nitrate uptake rate per surface area of sediment increased 10-fold when the thioplocas stretched out from the sediment as compared to a withdrawn state [9].

3.2 Coexistence with Beggiatoa

Although the thioplocas typically live in sheaths in bundles ranging from a few up to a hundred filaments per sheath, many were found at the sediment surface apparently without a sheath. At the Bay of Concepción on the Chilean coast, there was a transition between an apparently pure Beggiatoa community inside the bay to a mixed community of both genera at the entrance of the bay to pure Thioploca outside. In the mixed community it was not possible to discriminate beggiatoas from thioplocas (occurring outside their sheaths) by simple microscopy but only by analyzing statistically their diameter distributions. The tapered ends of filaments, characteristic of Thioploca but absent in Beggiatoa, was not a consistent character of the thioplocas. Often two or even three well-defined size classes of Thioploca occurred within the same sheath, e.g. T. araucae, T. chileae and T. marina together [13]. This is a puzzling phenomenon since inhabitants in one, unbranched sheath would be expected to represent a clone. A possible, although unconfirmed, explanation is that the filaments, which at the sediment surface, regularly stretch far out of their own sheath, adhere to other filaments and passively glide together with these down into different sheaths when those filaments retract. Too little is known about the physiology of individual Thioploca species to speculate what may be the functional relationships between different size classes when inhabiting the same sheath.

3.3 Biogeochemistry

Due to the extremely high phytoplankton productivity in the upwelling areas off the Pacific coast of South America, the organic sedimentation is correspondingly high. Carbon oxidation rates of up to 50 mmol C m−2 day−1 were measured in the uppermost 0–10 cm of sediment [20,33], principally as a result of sulfate reduction under the anoxic conditions (Fig. 4C). The measured sulfate reduction rates, with peak activities of up to 5 mM SO2−4 day−1 and areal rates of 25 mmol m−2 day−1 in the upper 0–10 cm, are among the highest found in any marine sediment. Yet, sulfate showed little depletion in the top 10–15 cm of sediment and the produced H2S barely accumulated to measurable concentrations (≤1 μM) in the porewater (Fig. 4D). This shows that the sulfide reoxidation was extremely rapid and efficient, even during summer in the complete absence of oxygen in the overlying water. Consequently, nitrate in the vacuoles of thioplocas appears to be the main oxidant for sulfide and is carried down into the sediment from the overlying water inside the vacuoles of vertically migrating thioplocas.

These results are in contrast to the findings by Henrichs and Farrington [35] from sediments underlying the oxygen minimum zone off the coast of Peru. Here, the thioplocas were surrounded by porewater with a rather high sulfide concentration and their H2S oxidation capacity was apparently insufficiently to keep pace with the similarly high sulfate reduction rates [36]. However, also off Peru the thioploca communities occurred under the oxygen minimum zone with <5 μM O2 and 35–45 μM NO3 in the overlying water column [35]. The absence of oxygen and availability of nitrate thus seem to be more important for the growth of Thioploca spp. than the surrounding sulfide concentration.

4 Ecology of Thioploca

4.1 Chemotaxis

Simple chemotactic responses may lead to a complex migration pattern of the whole Thioploca community, as demonstrated in intact sediment cores maintained under in situ conditions in an anoxic flume [9]. The organisms show a very distinct, positive reaction to nitrate and their emergence above the sediment surface could repeatedly be triggered by experimental addition of nitrate to the overflowing sea water. The thioplocas, however, react negatively to oxygen in the sea water, but the positive response to nitrate overrides the phobic response to oxygen at low O2 concentrations. The organisms thus appear to be strictly microaerophilic like the beggiatoas or may even preferentially grow anaerobically. The thioplocas showed a positive response to low sulfide concentrations, <100 μM, but a negative response to higher sulfide concentrations. Generally, the thioplocas appear to be more sensitive towards oxygen than the beggiatoas and tend to lyse some hours after exposure to air-saturated levels of oxygen. It is not yet clear how the combined chemotactic responses of Thioploca result in the formation of near-vertical sheaths penetrating deep down into the sediment and in their gliding movement from these deep tunnels up into the flowing seawater. Do the filaments continue moving in one direction until adverse conditions are sensed, or do they have spontaneous reversals similar to Beggiatoa[37]? When they stretch several cm up into the overflowing seawater, how do the long filaments sense when to stop, so that they do not lose contact with their sheath or are flushed away by the current? In fact, free Thioploca filaments have repeatedly been observed during plankton tows in the water column over the mats.

4.2 Ecological niche

By their oriented vertical migration and their ability to store large quantities of nitrate and sulfur in the cells, the large thioplocas occupy an ecological niche which is unique among prokaryotic communities. By transporting nitrate intracellularly deep down into the anoxic seafloor, Thioploca appears to effectively eliminate the competition from other sulfide oxidizing bacteria, which are unable to store an electron acceptor for extended periods but need concurrent access to both electron acceptor and donor in their immediate microenvironment. A similar storage of oxygen in the vacuoles would not be possible since the lipid membranes enclosing cells and vacuoles are permeable to gases. The thioplocas thus commute up and down, recharging their ‘lungs’ with nitrate at the surface and oxidizing sulfide at depth, thereby storing elemental sulfur globules as an energy reserve. By their special mode of life, the thioplocas also overcome the physical limitation of substrate availability, which for the beggiatoas and other H2S oxidizers is determined by the gradients of counter-diffusing sulfide and oxygen or nitrate [29,30]. Within the 1–2 cm thick mats of Thioploca, the combined structures of sheaths, polychaete tubes and pelletized sediment form a porous, spongy texture which is highly permeable to current-driven advective porewater flow [9,38]. Thus, nitrate decreased in the pore water from 25 μM at the sediment surface and to zero at 3–4 cm depth, so the dense bacterial community within the mat had a good access to nitrate-rich sea water.

4.3 Nitrogen metabolism

It remains to be shown whether the nitrate, which apparently serves as a respiratory electron acceptor, is used for denitrification or whether the thioplocas have a dissimilatory nitrate reduction to ammonia. Preliminary evidence points towards the latter (N.P. Revsbech and L.P. Nielsen, unpublished results). However, McHatton et al. [39] recently found that also the large Beggiatoa spp. living around hydrothermal vents contained nitrate-rich vacuoles. Assays for enzyme activity showed high activity of both RUBISCO, the CO2-fixing enzyme of the Calvin cycle, and of nitrate reductase, which led to the preliminary conclusion that these bacteria are autotrophic sulfide oxidizers using nitrate for respiration in a membrane-bound electron transport system. The presence of a dissimilatory nitrate metabolism in Beggiatoa is otherwise not clear. One strain was found to reduce nitrate to ammonium, although it did not grow in pure culture with nitrate as the electron acceptor [40]. Sweerts et al. [41] found that nitrate was consumed effectively in a freshwater mat of Beggiatoa, and in purified material from the mat denitrification could be demonstrated using 15N as a tracer. It was not proven, however, whether the conversion of  15NO3 to 15N2 was due to Beggiatoa or to contaminating bacteria. Evidence for nitrate respiration has recently been found in chemoautotrophic sulfide oxidizing bacteria living as symbionts in marine invertebrates [42].

4.4 Sulfur metabolism

It is not clear whether and how Thioploca, packed in their sheaths and penetrating deep into the sediment, can oxidize the ambient H2S so efficiently that the pore water sulfide concentration is kept below 1 μM (Fig. 4D). At such a low concentration, the diffusion gradients and thus the diffusive flux of H2S to the sheaths are correspondingly small. Data on the geochemical redox processes in the Chilean shelf sediments show that oxidized iron may also play an important role as an effective scavenger of H2S [33]. This still leaves the question of how the reduced iron is being reoxidized at a sufficient rate to continuously bind the sulfide. It is an interesting observation that the inhabited sheaths of Thioploca are densely covered by filamentous sulfate reducing bacteria of the genus Desulfonema (Fig. 1G). These are seen microscopically as thin filaments, longitudinally oriented on the outside of the sheaths, and they have been identified as Desulfonema by specific probes for fluorescent in situ hybridization (M. Fukui and F. Widdel, personal communication). The close proximity of these sulfate reducing Desulfonema and the sulfide oxidizing Thioploca may help to explain how such a rapid recycling of H2S can take place.

5 Global occurrence

By their great extension and biomass, their highly efficient nitrate scavenging, and their coupling of the nitrogen, sulfur and carbon cycles the thioplocas may play an important role in the biogeochemistry of marine upwelling regions. Whether they contribute significantly to the intensive denitrification in these regions still remains to be proven. The biomass of the Thioploca population is positively related to high sedimentation rates of organic matter and to oxygen depletion. Thus, the bacteria depend indirectly on the local primary productivity and the intensity of upwelling. Off the coast of Chile and Peru, the Thioploca biomass was low during winter and high during summer and early fall when organic deposition was highest and the bottom water oxygen concentrations remained below a few percent of air saturation [34,43,44]. In accordance with this, a general decrease in Thioploca biomass was noted during ‘El Niño’ years, when the regional wind and current systems impeded upwelling and oxygen depletion. Marine Thioploca communities have recently also been found in other areas of intense upwelling and of oxygen-poor bottom water. In the northwest Arabian Sea, the monsoon-driven upwelling combined with the inflow of poorly oxygenated waters from the Red Sea creates an oxygen minimum zone at 100–1000 m water depth. Sheaths with 30–40 μm wide Thioploca were found abundantly in the sediment at about 400 m depth [45]. Along the south-western coast of the African continent, Thioploca has been found in sediments off the coast of Namibia where the highly productive upwelling ecosystem of the Benguela Current causes oxygen depletion over the shelf ([46] and H.N. Schulz, unpublished observations). Thioplocas have also been found to inhabit the sea floor around hydrothermal vents in the eastern Mediterranean Sea [47]. Further habitats continue to be recorded and large populations have recently also been found in lakes, e.g. the Russian Lake Baikal [48] and the Japanese Lake Biwa [49]. As renewed interest is focused on these extraordinary bacteria, their occurrence appears to be much more widespread than previously thought and they probably play a significant role in the biogeochemistry of many anoxic sediments.


We thank the following colleagues for their kind permission to present their unpublished photographs and results: Michael A. Arthur, Manabu Fukui, Markus Huettel, Sigfried Maier, Thomas Neu, Lars Peter Nielsen, Niels Peter Revsbech, Heide Schulz, Andreas Teske and Horst Voelker. Our research on the marine thioplocas has been funded by the Chilean FONDECYT and FONDAP Programs and by the German Max Planck Society.


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