A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents

Abstract

Deep-sea hydrothermal vents play an important role in global biogeochemicalcycles, providing biological oases at the seafloor that are supported by the thermal and chemical flux from the Earth's interior. As hot, acidic and reduced hydrothermal fluids mix with cold, alkaline and oxygenated seawater, minerals precipitate to form porous sulphide-sulphate deposits. These structures provide microhabitats for a diversity of prokaryotes that exploit the geochemical and physical gradients in this dynamic ecosystem 1 Table 2, Supplementary Fig. S1). The DHVE2 were identified in 36 samples and represented up to 10 and 15% of the archaeal population at EPR and ELSC, respectively (as determined by quantitative PCR; Table 1). Generally, the occurrence of DHVE2 appeared to be associated with the fine-grained white elemental sulphur, S 8 , (identified in three different samples by X-ray diffraction, Supplementary Methods) or iron oxyhydroxide (X-ray amorphous -identified based on orange color and texture, Supplementary Table 3) deposits that often coat the outside of mature actively venting sulphide deposits ( Supplementary Fig. S2). Additionally, due to the high guanine and cytosine content of the 16S rRNA sequence and its occasional co-occurrence with thermophiles such as Thermococcus, it has been suggested that the DHVE2 are thermophiles, perhaps heterotrophs whose growth may be stimulated by sulphur 1,16 . A DHVE2 genome fragment from a metagenome library contained a thermostable DNA polymerase, which was further suggestive of the thermophilic nature of this lineage 17 . However, all attempts to culture this group using standard media and conditions to select for sulphate reducers, methanogens or fermenters at 60, 80 and 90°C and around pH 6.5 have been unsuccessful 5 .Based on the predictions that conditions within many sulphide deposits should be acidic, and due to the presence of novel sequences most closely related to the acidophiles, Thermoplasma, Picrophilus and Ferroplasma (Fig. 1 The cells are pleiomorphic to spherical, about 0.6-1 µm in diameter and are motile with a single flagellum (Fig. 2a, b). Some flagella have their proximal end encased in an unusual complex periodic sheath (Fig. 2c). Like many other Archaea (e.g.Methanococcus and Sulfolobus), they are enveloped by a plasma membrane and a single S-layer (Fig. 2a, e). The S-layer, similar to that of Picrophilus oshimae 23 , is thick (~40nm), with a presumed tetragonal (p4) lattice and resembles a delicate bridal veil bordering the cells (Fig. 2a). Although S-layers are quasi-crystalline this S-layer bends into small highly curved structures (Fig. 2d, vesicles). These vesicles bud from the cell partitioning small quantities of cytoplasm that could then anneal to adjacent cells. This is a process that is common amongst their Gram-negative bacterial counterparts 24 . The ability of DHVE2's S-layer to bend into such high curvature structures as these vesicles,suggests that the bonding forces between S-layer subunits are weak or transient. This is unusual 25 ,...

Hindsight in the relative abundance, metabolic potential and genome dynamics of uncultivated marine archaea from comparative metagenomic analyses of bathypelagic plankton of different oceanic regions

“…From the 10 euryarchaeotal genomic clones sequenced, 3 were ascribed to the Group III and the rest to deep-sea Group II members, as none of the 16S rDNA sequences from our libraries branched with the phototrophic euryarchaeota Comparative metagenomics of deep-sea archaea A-B Martin-Cuadrado et al . The recently isolated Aciduliprofundum boonei, an obligate thermoacidophilic sulphur-or iron-reducing heterotrophic deep-sea vent archaeon representative of the DHVE2 group (Reysenbach et al, 2006), branched closer to the Thermoplasmatales than to the Groups II and III ( Figure 3 and data not shown). As in the case of crenarchaeota, we sequenced fosmids from the same pan-oceanic OTUs coming from at least one Mediterranean and one South Atlantic or Antarctic location.…”

Chemolithotrohic Bacteria: Distributions, Functions and Significance in Volcanic Environments

“…These systems have yielded a rich variety of novel chemolithotrophs 1,9,15,57,65,76,77,79,87) capable of exploiting the typically high concentrations of reduced inorganic substrates (especially various sulfur species) associated with many volcanic environments. The properties of many of these isolates have been unexpected, and opened new horizons in microbial biology 35,39,70,84) .…”

A new class of marine Euryarchaeota group II from the mediterranean deep chlorophyll maximum

“…MG2-GG3, similar to many other marine prokaryotes, seems to be a photoheterotroph, possessing a rhodopsin to collect light energy but with the hallmarks of a heterotrophic lifestyle. The existence of many large peptidases, similar to the ubiquitous thermoacidophilic archaeon Aciduliprofundum boonei, a known protein degrader from deep-sea hydrothermal vents (Reysenbach et al, 2006), suggested that proteins may be important substrates for this microbe. Moreover, the presence of a complete fatty acid degradation pathway, together with proteins with a variety of adhesion domains and a type II/IV secretion systems to transport such proteins to the cell surface, led the authors to suggest a particle-associated lifestyle.…”