Thioploca araucae

A Microbial Biorealm page on the genus Thioploca araucae

Classification

Cellular Organisms; Bacteria; Proteobacteria; Gammaproteobacteria; Thiotrichales; Thiotrichaceae; Thioploca

Species

NCBI: Taxonomy

Thioploca araucae

Description and significance

Thioploca araucae is a filamentous sulfur-oxidizing bacteria that usually lives in bundles that are surrounded by a sheath. The cells, which are roughly 60 um long and 40 um wide, form thick bacterial mats on the sea floor below the oxygen-minimum zone in upwelling regions of the ocean. Water depths between 40 and 280 meters are common for these areas. (1) The continental shelf off the coast of Chile and southern Peru is one such upwelling region, and is where V.A. Gallardo first discovered Thioploca spp. in 1977. (5) This marine discovery of Thioploca was well after the first discoveries of other Thioploca species in freshwater lakes and ponds. (4) Thioploca sheaths reach a maximum wet weight of 800 grams per meter at a depth of 90 meters. The actual bacterial filaments inside of these sheaths are 10% of the weight, while about 20% of sheaths contain more than one kind of Thioploca species. (3) Thioploca araucae is important in that it serves as a bridge between the nitrogen and sulfur cycles. It reduces nitrate into elemental sulfur and then sulfate, linking the two cylces in the sediment. While Thioploca araucae is not unique in this respect, it is in that it can store both nitrate and sulfur within its cells. This makes its survival independent of coexisting substrates. (1)

(The first sulfur bacteria Thioploca spp. were found in freshwater lakes and ponds (4). Then, in 1977, V.A. Gallardo discovered Thioploca spp. on the seabed off the coast of Chile and Peru (5). Thioploca araucae is among the two species of marine Thioploca spp. that is present in these populations.)

(Thioploca sheaths and filaments were found across the whole shelf area within the oxygen minimum zone. The maximum wet weight of sheaths, 800 g m22, was found at a depth of 90 m. The bacterial filaments within the sheaths accounted for 10% of this weight.(3))

(Marine species of Thioploca occur over 3,000 km along the continental shelf off Southern Peru and North and Central Chile. These filamentous bacteria live in bundles surrounded by a common sheath and form thick mats on the sea floor under the oxygen-minimum zone in the upwelling region, at between 40 and 280 m water depth. It serves as a bridge between the nitrogen and sulfur cycles.) After taking in nitrage, gliding filaments transport this nitrate 5–10 cm down into the sediment and reduce it, with concomitant oxidation of hydrogen sulphide, thereby coupling the nitrogen and sulphur cycles in the sediment (1).

Genome structure

The genome is currently being sequenced as part of the Moore Foundation Microbial Genome Sequencing project. A sample collected by Victor Gallardo on the continental shelf off of Concepcion, Chile is being studied by the J Craig Venter Institute. Data from 16S rRNA analysis suggests that Beggiatoa is Thioploca's closest phylogenetic relative. Thioploca and Beggiatoa form a phylogenetic lineage within the gamma-subdivision of the proteobacteria, showing similar genetic diversity that other groups of sulfur oxidizers have. Often differentiated simply by size, fluorescent in situ hybridization with Thioploca-specific oligonucleotide probes can used to separate the sequences of Thioploca araucae and Thioploca chileae. (10)

Cell structure and metabolism

The network of interwoven horizontal sheaths that is held in place by the root-like vertical sheaths stabilizes the sediment very efficiently.(3)

Thioploca araucae contain light-refracting sulfur globules in their cytoplasm that surround a large vacuole. This vacuole is used to concentrate nitrate at levels up to 500 mM and can occupy greater than 80% of the cell's volume.(1) Gliding filaments serve to trasport this nitrate 5-10 cm down into the sediment, where it will be reduced.(3) A sequence of reactions is then carried out in order to reduce nitrate and oxidize sulfur. First, hydrogen sulfide is oxidized using the nitrate, resulting in the production of elemental sulfur that is stored in the cytoplasm in the form of the sulfur globules. This reaction is thought to be: 2NO3- + 5HS + 7H+ --> N2 + 5S + 6H2O. The elemental sulfur is then oxidized, resulting in sulfate: 6NO3- + 5S + 2H2O --> 3N2 + 5(SO4)2 + 4H+. The sulfur compound hydrogen sulfide serves as a source of electrons for bacterial chemosynthesis, while the oxidation of sulfur serves as the source of energy instead of light.The result of this is a linking of the nitrogen and sulfur cycles.

These results suggest that Thioploca species are facultative chemolithoautotrophs capable of mixotrophic growth

Ecology

Thioploca cells form filaments that cling to each other and secrete an encompassing sheath of mucous film. The sheath serves as a kind of vertical tunnel through the sediment up to the overlying water, allowing the Thioploca filaments to glide up and down and thereby commute between their food source and the nitrate they need to metabolize it. Thioploca araucae and its sheaths is often mixed in with other bacteria. Among these is Thioploca chileae, the other marine species of Thioploca. In 85% of the sheaths that have mixed populations, Thioploca araucae is usually more widespread. In fact, the Thioploca araucae population is larger in both biomass and number than the Thioploca chileae population (3).

It is estimated that close to one-quarter of global marine denitrification is done in the upwelling waters off the Pacific coast of South America (2). Thioploca araucae, along with other sulfur oxidizers such as Beggiatoa, plays a major role in this.

Close physical associations between filamentous sulfur-oxidizing bacteria and filamentous δ-proteobacteria have been observed in organic-rich marine and lacustrine surface sediments, where Desulfonema filaments are epibionts on large sulfur-oxidizing filaments such as Thioploca spp. (8)

Pathology

None found.

Application to Biotechnology

Does this organism produce any useful compounds or enzymes? What are they and how are they used?

Current Research

Most current research involves studying what conditions are favored by Thioploca araucae, its actual method of metabolizing sulfur and nitrogen, and the ongoing quest for its genome.

energy yields of nitrate reduction are far lower than one would expect from the free energy changes of the overall redox reactions (delta g)

it appears that about twice as much cell mass can be synthesized per mol nitrate by nitrate ammonification as by denitrification (15.6 versus 7.6 g per nitrate reduced with formate as electron donor

all recently described lithotrophic bacteria oxidizing sulfide with nitrate as electron acceptor at neutral pH, e.g., Thioploca sp. or Thiomargarita sp., convert nitrate to ammonia (12, 16, 17), although denitrification should provide them with more energy. Thus, it is not surprising that nitrate ammonification is the preferred nitrate respiration process under conditions of nitrate limitation (26) and that especially lithoautotrophic sulfide oxidation by, e.g., Thioploca sp. or Thiomargarita sp. prefers nitrate ammonification over denitrification (6).

The closely related genera Beggiatoa, Thioploca, and Thiomargarita are among the largest prokaryotes known, and they usually contain a vacuole that can account for up to 90% of the cell volume. On the seafloor these large sulfur-oxidizing bacteria fulfill an important ecological function by preventing the release of toxic hydrogen sulfide from the sediment into the water column. Oxygen has been regarded as the major electron acceptor coupled to sulfur oxidation; however, there is growing evidence that when experiencing anoxia these large vacuolated Beggiatoa, Thioploca, and Thiomargarita respire nitrate, which they concentrate up to 10,000-fold (~500 mM) within their intracellular vacuoles Under nutritional imbalance many bacteria accumulate phosphate, which is intracellularly stored as polyP. Thiomargarita and Thioploca exhibit an efficient phosphate uptake and storage system and contain large polyP granules. Recently, these organisms were hypothesized to account for large phosphorite deposits at the sea floor

problems to overcome when sequencing genome" We have shown that the combination of optical mapping, WGA, and pyrosequencing offers great potential for genomic analysis of individual, uncultured bacteria. However, the incomplete sequence assemblies limited the accurate determination of the genome size and an in-depth analysis of the Beggiatoa genome. Generally, the contribution of non-target DNA cannot be completely ruled out in environmental WGA projects (7).

References

1. H. Fossing, V.A. Gallardo, et. al. "Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca". Nature. 1995. Volume 374. p.713-715.

2. Codispoti, L.A. et al. Science. 1986. Volume 233. p.1200-1202.

3. Schulz, H., Jorgensen, B., Fossing, H., and Ramsing, N. "Community Structure of Filamentous, Sheath-Building Sulfur Bacteria, Thioploca spp., off the Coast of Chile". Applied and Environmental Microbiology. 1996. Volume 62. p. 1855-1862.

4. Lauterborn, R. "Eine neue Gattung der Schwefelbakterien (Thioploca Schmidlei nov. gen. nov. spec.)". Ber. Dtsch. Bot. Ges. 1907. Volume 25. p.238–242.

5. Gallardo, V. A. "Large benthic microbial communities in sulphide biota under Peru-Chile Subsurface Countercurrent". Nature (London). 1997. Volume 268. p.331–332.

6. Strohm, T., Griffin, B., Zumft, W., and Schink, B. "Growth Yields in Bacterial Denitrification and Nitrate Ammonification". Applied and Environmental Microbiology. 2007. Volume 73(5). p. 1420-1424.

7. Mußmann, M., Hu, F., Richter, M., et al. "Insights into the Genome of Large Sulfur Bacteria Revealed by Analysis of Single Filaments". PLoS Biology. 2007. Volume 5(9). e230.

8. Macalady, J., et al. "Dominant Microbial Populations in Limestone-Corroding Stream Biofilms, Frasassi Cave System, Italy". Applied and Environmental Microbiology. 2006. Volume 72(8). p. 5596-5609.

9. Jørgensen, B. and Gallardo, V. "Thioploca spp. filamentous sulfur bacteria with nitrate vacuoles". FEMS Microbiology Ecology. 1999. Volume 28(4), p. 301-313.

10. Teske, A. P., N. B. Ramsing, J. Ku¨ver, and H. Fossing. 1995. Phylogeny of Thioploca and related filamentous sulfide-oxidizing bacteria. Syst. Appl. Microbiol. 18:517–526.

Edited by student of Rachel Larsen

Nitrogen, Carbon, and Sulfur Metabolism in Natural Thioploca Samples

Vertical Migration in the Sediment-Dwelling Sulfur Bacteria Thioploca spp. in Overcoming Diffusion Limitations MARKUS HUETTEL,* STEFAN FORSTER, SUSANNE KLO¨ SER, AND HENRIK FOSSING Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany

Population study of the filamentous sulfur bacteria Thioploca spp. off the Bay of Concepcion, Chile Heide N. Schulzl~*B, ettina Strotmannl, Victor A. Gallardo2, Bo B. ~ergensen' 'Max Planck Institute for Marine Microbiology, Celsiusstrasse 1.28359 Bremen, Germany

Maier S & Gallardo VA (1984) Maier, S., and Gallardo, V.A. "Thioploca araucae sp. nov. and Thioploca chileae sp. nov." Int. J. Syst. Bacteriol. (1984) 34:414-418. [No PubMed record available.]