Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography

Junglas, Benjamin; Briegel, Ariane; Burghardt, Tillmann; Walther, Paul; Wirth, Reinhard; Huber, Harald; Rachel, Reinhard

doi:10.1007/s00203-008-0402-6

Cited by 73 publications

(76 citation statements)

References 46 publications

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“…This interaction could involve injection of nutrients from Thermoplasmatales cells into ARMAN, parasitism of ARMAN, or exchange of molecules between them. Notable features distinguishing ARMAN-Thermoplasmatales interactions from those reported previously for N. equitans and I. hospitalis (10,11,14) include the rarity of cell-to-cell interactions and the cytoplasmic connection between ARMAN and the associated cell.…”

Section: Resultsmentioning

confidence: 74%

“…The ultrasmall archaeal parasite Nanoarchaeum equitans has only 552 genes and requires a connection to its archaeal host, Ignicoccus hopstialis, to survive (10). Recently, it was shown that this interaction involves contact between outer membranes (14). Given the vast diversity of microbial life (15), it is likely that other unusual relationships critical to survival of organisms and communities remain to be discovered.…”

mentioning

confidence: 99%

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Enigmatic, ultrasmall, uncultivated Archaea

Baker¹,

Comolli

Dick³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

314

296

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Metagenomics has provided access to genomes of as yet uncultivated microorganisms in natural environments, yet there are gaps in our knowledge-particularly for Archaea-that occur at relatively low abundance and in extreme environments. Ultrasmall cells (<500 nm in diameter) from lineages without cultivated representatives that branch near the crenarchaeal/euryarchaeal divide have been detected in a variety of acidic ecosystems. We reconstructed composite, near-complete ∼1-Mb genomes for three lineages, referred to as ARMAN (archaeal Richmond Mine acidophilic nanoorganisms), from environmental samples and a biofilm filtrate. Genes of two lineages are among the smallest yet described, enabling a 10% higher coding density than found genomes of the same size, and there are noncontiguous genes. No biological function could be inferred for up to 45% of genes and no more than 63% of the predicted proteins could be assigned to a revised set of archaeal clusters of orthologous groups. Some core metabolic genes are more common in Crenarchaeota than Euryarchaeota, up to 21% of genes have the highest sequence identity to bacterial genes, and 12 belong to clusters of orthologous groups that were previously exclusive to bacteria. A small subset of 3D cryo-electron tomographic reconstructions clearly show penetration of the ARMAN cell wall and cytoplasmic membranes by protuberances extended from cells of the archaeal order Thermoplasmatales. Interspecies interactions, the presence of a unique internal tubular organelle [Comolli, et al. (2009) (1)]. Many datasets provide fragmentary glimpses into genetic diversity (2-4) and a few have reported near-complete genomic sequences for uncultivated organisms (5-8). In most cases where extensive reconstruction has been possible, insights have been restricted to relatively dominant members. Furthermore, it has been difficult to use genomic information to infer the nature of interorganism interactions, although these are likely to be very important aspects of microbial community functioning. The need for topological and organizational information to place genomic data in context motivates the combination of cultivation-independent genomics and 3D cryogenic transmission electron microscope-based ultrastructural analyses of microbial communities.Despite the importance of cellular interactions (symbiosis and parasitism), most of what we know about microorganismal associations is from cultivation-based studies (9-11). However, sequencing of the genomes of several endosymbiotic and parasitic Bacteria has revealed reduction in gene and genome sizes, reflecting evolved dependence of the endosymbiont or parasite on its host (12, 13). The ultrasmall archaeal parasite Nanoarchaeum equitans has only 552 genes and requires a connection to its archaeal host, Ignicoccus hopstialis, to survive (10). Recently, it was shown that this interaction involves contact between outer membranes (14). Given the vast diversity of microbial life (15), it is likely that other unusual relationships critical to surviva...

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Section: Resultsmentioning

confidence: 74%

mentioning

confidence: 99%

Enigmatic, ultrasmall, uncultivated Archaea

Baker¹,

Comolli

Dick³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

314

296

View full text Add to dashboard Cite

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“…These two membranes enclose an intermembrane compartment with a variable width from 20 to 500 nm, resulting in a volume exceeding that of the cytoplasm (5). Its low electron density suggests that it is devoid of cellular material like ribosomes or DNA, and it was therefore named "periplasm" (7). The inner membrane, called the cytoplasmic membrane, releases numerous vesicles into the periplasmic space and also engulfs vesicles into the cytoplasm (7).…”

Section: T He Hyperthermophilic Crenarchaeon Ignicoccus Hospitalis Kimentioning

confidence: 99%

Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis

Küper

Meyer

Müller

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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ATP synthase catalyzes ATP synthesis at the expense of an electrochemical ion gradient across a membrane that can be generated by different exergonic reactions. Sulfur reduction is the main energyyielding reaction in the hyperthermophilic strictly anaerobic Crenarchaeon Ignicoccus hospitalis. This organism is unusual in having an inner and an outer membrane that are separated by a huge intermembrane compartment. Here we show, on the basis of immuno-EM analyses of ultrathin sections and immunofluorescence experiments with whole I. hospitalis cells, that the ATP synthase and H 2 :sulfur oxidoreductase complexes of this organism are located in the outer membrane. These two enzyme complexes are mandatory for the generation of an electrochemical gradient and for ATP synthesis. Thus, among all prokaryotes possessing two membranes in their cell envelope (including Planctomycetes, Gram-negative bacteria), I. hospitalis is a unique organism, with an energized outer membrane and ATP synthesis within the periplasmic space. In addition, DAPI staining and EM analyses showed that DNA and ribosomes are localized in the cytoplasm, leading to the conclusion that in I. hospitalis energy conservation is separated from information processing and protein biosynthesis. This raises questions regarding the function of the two membranes, the interaction between these compartments, and the general definition of a cytoplasmic membrane.Archaea | ATP synthase | ATPase | immunolabeling | sulfur reductase

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“…Cells were prepared for transmission electron microscopy as described in detail elsewhere (7,28). In brief, for visualizing whole cells, cells in suspension were chemically fixed by adding glutaraldehyde (final concentration, 2%), concentrated by brief centrifugation, applied to carbon-coated copper grids, and shadowed with 1 nm Pt/C (angle, 15°).…”

Section: Rhodopirellulamentioning

confidence: 99%

Determination of the Diversity of Rhodopirellula Isolates from European Seas by Multilocus Sequence Analysis

Winkelmann

Jaekel

Meyer

et al. 2010

Appl Environ Microbiol

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In the biogeography of microorganisms, the habitat size of an attached-living bacterium has never been investigated. We approached this theme with a multilocus sequence analysis (MLSA) study of new strains of Rhodopirellula sp., an attached-living planctomycete. The development of an MLSA for Rhodopirellula baltica enabled the characterization of the genetic diversity at the species level, beyond the resolution of the 16S rRNA gene. The alleles of the nine housekeeping genes acsA, guaA, trpE, purH, glpF, fumC, icd, glyA, and mdh indicated the presence of 13 genetically defined operational taxonomic units (OTUs) in our culture collection. The MLSA-based OTUs coincided with the taxonomic units defined by DNA-DNA hybridization experiments. BOX-PCR supported the MLSA-based differentiation of two closely related OTUs. This study established a taxon-area relationship of cultivable Rhodopirellula species. In European seas, three closely related species covered the Baltic Sea and the eastern North Sea, the North Atlantic region, and the southern North Sea to the Mediterranean. The last had regional genotypes, as revealed by BOX-PCR. This suggests a limited habitat size of attached-living Rhodopirellula species.The biogeography of microorganisms describes the habitat size of the species and the distribution of microorganisms on Earth. The experimental approaches depend on the focus of the studies. Habitats are often analyzed by environmental microbiologists with genetic-fingerprinting techniques, with up to 200 bands or fragments representing the whole community. Although the taxonomic resolution of these operational taxonomic units (OTUs) is limited, the studies revealed a community biogeography (22). Medical microbiologists analyze the alleles of housekeeping genes of microorganisms to gain insight into the epidemiology of pathogens, the population biogeography (2). This strain-specific, fine-scale taxonomic resolution within a species is well suited to observance of recent dispersal events. At the species level, multilocus sequence typing (MLST) and analysis (MLSA), which were developed for intraspecies and intragenus specific studies, respectively, consist of the sequences of several (at least seven) housekeeping gene fragments concatenated to an approximately 5-kilobase alignment (17). Recent MLSA studies revealed its applicability to marine isolates and the analysis of biogeographic patterns: Alteromonas macleodii isolates could be grouped in an epipelagic and an abyssal clade (6), and strains of Pseudomonas aeruginosa were genetically well separated into groups of coastal and oceanic origin (8). However, for Salinibacter ruber strains, biogeographical distinctness was not resolved in an MLSA study but showed allopatry in a metabolic analysis (31). Several studies used MLSA together with DNA-DNA hybridization (DDH) for the delineation of new species, e.g., for Vibrio and Ensifer spp. (20,36).In the biogeography of microorganisms, the experimental proof of a local genetic evolution was first revealed at sample sites...

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Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography

Cited by 73 publications

References 46 publications

Enigmatic, ultrasmall, uncultivated Archaea

Enigmatic, ultrasmall, uncultivated Archaea

Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis

Determination of the Diversity of Rhodopirellula Isolates from European Seas by Multilocus Sequence Analysis

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