Archaeal Richmond Mine acidophilic nanoorganisms

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ARMAN (uncultured acidophilic lineages)
25K15pA9Def4sec Arman 4 Box1.png
Scientific classification
Domain:
Archaea
Phylum:
Micrarchaeota Parvarchaeota

Archaeal Richmond Mine acidophilic nanoorganisms (ARMAN) were first discovered in an extremely acidic mine located in northern California (Richmond Mine at Iron Mountain) by Brett Baker in Jill Banfield's laboratory at the University of California Berkeley. These novel groups of archaea named ARMAN-1, ARMAN-2 ( Candidatus Micrarchaeum acidiphilum ARMAN-2), and ARMAN-3 were missed by previous PCR-based surveys of the mine community because the ARMANs have several mismatches with commonly used PCR primers for 16S rRNA genes. Baker et al. [1] detected them in a later study using shotgun sequencing of the community. The three groups were originally thought to represent three unique lineages deeply branched within the Euryarchaeota, a subgroup of the Archaea. However, based on a more complete archaeal genomic tree, they were assigned to a new superphylum named DPANN. [2] The ARMAN groups now comprise deeply divergent phyla named Micrarchaeota and Parvarchaeota. [3] Their 16S rRNA genes differ by as much as 17% between the three groups. Prior to their discovery, all of the Archaea shown to be associated with Iron Mountain belonged to the order Thermoplasmatales (e.g., Ferroplasma acidarmanus ).

Contents

Distribution

Examination of different sites in the mine using fluorescent probes specific to the ARMAN groups has revealed that they are always present in communities associated with acid mine drainage (AMD), at Iron Mountain in northern California, that have pH < 1.5. They are usually found in low abundance (5–25%) in the community. Recently, closely related organisms have been detected in an acidic boreal mire or bog in Finland, [4] another acid mine drainage site in extreme environments of Rio Tinto, southwestern Spain, [5] and at a weak-alkaline deep subsurface hot spring in Yunohama, Japan. [6]

Cell structure and ecology


Using cryo-electron tomography, a 3D characterization of uncultivated ARMAN cells within mine biofilms [7] revealed that they are right at the cell size predicted[ citation needed ] to be the lower limit for life, 0.009 μm3 and 0.04 μm3. Despite their unusually small cell size it is common to find more than one type of virus attached to the cells while in the biofilms. Furthermore, the cells contain on average ≈92 ribosomes per cell, whereas the average E. coli cell grown in culture contains ≈10,000 ribosomes. This suggests that for ARMAN cells a much more limited number of metabolites are present in a given cell. It raises questions about what the minimal requirements are for a living cell.

3D reconstructions of ARMAN cells in the environment has revealed that a small number of them attach to other Archaea of the order Thermoplasmatales (Baker et al. 2010 [8] ). The Thermoplasmatales cells appear to penetrate the cell wall to the cytoplasm of the ARMAN cells. [9] The nature of this interaction hasn't been determined. It could be some sort of parasitic or symbiotic interaction. It is possible that ARMAN is getting some sort of metabolite that it is not able to produce on its own.

Genomics and proteomics

The genomes of three ARMAN groups were sequenced at the DOE Joint Genome Institute during a 2006 Community Sequencing Program. [10] These three genomes were successfully binned from the community genomic data using ESOM or Emergent Self-Organizing Map clustering of tetranucleotide DNA signatures. [11]

The first draft of Candidatus Micrarchaeum acidiphilum ARMAN-2 is ≈1 Mb. [8] The ARMAN-2 has recently been closed using 454 and Solexa sequencing of other biofilms to close the gaps and is being prepared for submission to NCBI. The genomes of ARMAN-4 and ARMAN-5 (roughly 1 Mb as well) have unusually small average gene lengths, similar to those seen in endosymbiotic and parasitic bacteria. This may be signature of their interspecies interactions with other Archaea in nature. [8] Furthermore, the branching of these groups near the Euryarchaea/Crenarchaea divide is reflected in them sharing many genetic aspects of both Crenarchaea and Euryarchaea. Specifically they have many genes that had previously only been identified in Crenarchaea. It is difficult to elucidate many of the commonly known metabolic pathways in ARMAN due to the unusually high number of unique genes that have been identified in their genomes.

A novel type of tRNA splicing endonuclease, involved in the processing of tRNA, has been discovered in ARMAN groups 1 and 2. [12] The enzyme consists of two duplicated catalytic units and one structural unit encoded on a single gene, representing a novel three-unit architecture.

Related Research Articles

<i>Nanoarchaeum equitans</i> Species of archaeon

Nanoarchaeum equitans is a species of marine archaea that was discovered in 2002 in a hydrothermal vent off the coast of Iceland on the Kolbeinsey Ridge by Karl Stetter. It has been proposed as the first species in a new phylum, and is the only species within the genus Nanoarchaeum. Strains of this microbe were also found on the Sub-polar Mid Oceanic Ridge, and in the Obsidian Pool in Yellowstone National Park. Since it grows in temperatures approaching boiling, at about 80 °C (176 °F), it is considered to be a thermophile. It grows best in environments with a pH of 6, and a salinity concentration of 2%. Nanoarchaeum appears to be an obligate symbiont on the archaeon Ignicoccus; it must be in contact with the host organism to survive. Nanoarchaeum equitans cannot synthesize lipids but obtains them from its host. Its cells are only 400 nm in diameter, making it the smallest known living organism, and the smallest known archaeon.

<span class="mw-page-title-main">Nanoarchaeota</span> Phylum of archaea

Nanoarchaeota is a proposed phylum in the domain Archaea that currently has only one representative, Nanoarchaeum equitans, which was discovered in a submarine hydrothermal vent and first described in 2002.

<span class="mw-page-title-main">Korarchaeota</span> Proposed phylum within the Archaea

The Korarchaeota is a proposed phylum within the Archaea. The name is derived from the Greek noun koros or kore, meaning young man or young woman, and the Greek adjective archaios which means ancient. They are also known as Xenarchaeota. The name is equivalent to Candidatus Korarchaeota, and they go by the name Xenarchaeota or Xenarchaea as well.

<span class="mw-page-title-main">Euryarchaeota</span> Phylum of archaea

Euryarchaeota is a kingdom of archaea. Euryarchaeota are highly diverse and include methanogens, which produce methane and are often found in intestines; halobacteria, which survive extreme concentrations of salt; and some extremely thermophilic aerobes and anaerobes, which generally live at temperatures between 41 and 122 °C. They are separated from the other archaeans based mainly on rRNA sequences and their unique DNA polymerase.

Methanogens are anaerobic archaea that produce methane as a byproduct of their energy metabolism, i.e., catabolism. Methane production, or methanogenesis, is the only biochemical pathway for ATP generation in methanogens. All known methanogens belong exclusively to the domain Archaea, although some bacteria, plants, and animal cells are also known to produce methane. However, the biochemical pathway for methane production in these organisms differs from that in methanogens and does not contribute to ATP formation. Methanogens belong to various phyla within the domain Archaea. Previous studies placed all known methanogens into the superphylum Euryarchaeota. However, recent phylogenomic data have led to their reclassification into several different phyla. Methanogens are common in various anoxic environments, such as marine and freshwater sediments, wetlands, the digestive tracts of animals, wastewater treatment plants, rice paddy soil, and landfills. While some methanogens are extremophiles, such as Methanopyrus kandleri, which grows between 84 and 110°C, or Methanonatronarchaeum thermophilum, which grows at a pH range of 8.2 to 10.2 and a Na+ concentration of 3 to 4.8 M, most of the isolates are mesophilic and grow around neutral pH.

<i>Ferroplasma</i> Genus of archaea

Ferroplasma is a genus of Archaea that belong to the family Ferroplasmaceae. Members of the Ferroplasma are typically acidophillic, pleomorphic, irregularly shaped cocci.

Pyrobaculum is a genus of the Thermoproteaceae.

<span class="mw-page-title-main">Archaea</span> Domain of single-celled organisms

Archaea is a domain of single-celled organisms. These microorganisms lack cell nuclei and are therefore prokaryotic. Archaea were initially classified as bacteria, receiving the name archaebacteria, but this term has fallen out of use.

<span class="mw-page-title-main">Nitrososphaerota</span> Phylum of archaea

The Nitrososphaerota are a phylum of the Archaea proposed in 2008 after the genome of Cenarchaeum symbiosum was sequenced and found to differ significantly from other members of the hyperthermophilic phylum Thermoproteota. Three described species in addition to C. symbiosum are Nitrosopumilus maritimus, Nitrososphaera viennensis, and Nitrososphaera gargensis. The phylum was proposed in 2008 based on phylogenetic data, such as the sequences of these organisms' ribosomal RNA genes, and the presence of a form of type I topoisomerase that was previously thought to be unique to the eukaryotes. This assignment was confirmed by further analysis published in 2010 that examined the genomes of the ammonia-oxidizing archaea Nitrosopumilus maritimus and Nitrososphaera gargensis, concluding that these species form a distinct lineage that includes Cenarchaeum symbiosum. The lipid crenarchaeol has been found only in Nitrososphaerota, making it a potential biomarker for the phylum. Most organisms of this lineage thus far identified are chemolithoautotrophic ammonia-oxidizers and may play important roles in biogeochemical cycles, such as the nitrogen cycle and the carbon cycle. Metagenomic sequencing indicates that they constitute ~1% of the sea surface metagenome across many sites.

Nitrososphaera is a mesophilic genus of ammonia-oxidizing Crenarchaeota. The first Nitrososphaera organism was discovered in garden soils at the University of Vienna leading to the categorization of a new genus, family, order and class of Archaea. This genus is contains three distinct species: N. viennensis, Ca. N. gargensis, and Ca N. evergladensis. Nitrososphaera are chemolithoautotrophs and have important biogeochemical roles as nitrifying organisms.

The "Aigarchaeota" are a proposed archaeal phylum of which the main representative is Caldiarchaeum subterraneum. It is not yet clear if this represents a new phylum or a Nitrososphaerota order, since the genome of Caldiarchaeum subterraneum encodes several Nitrososphaerota-like features. The name "Aigarchaeota" comes from the Greek αυγή, avgí, meaning "dawn" or "aurora", for the intermediate features of hyperthermophilic and mesophilic life during the evolution of its lineage.

<span class="mw-page-title-main">Lokiarchaeota</span> Phylum of archaea

Lokiarchaeota is a proposed phylum of the Archaea. The phylum includes all members of the group previously named Deep Sea Archaeal Group, also known as Marine Benthic Group B. Lokiarchaeota is part of the superphylum Asgard containing the phyla: Lokiarchaeota, Thorarchaeota, Odinarchaeota, Heimdallarchaeota, and Helarchaeota. A phylogenetic analysis disclosed a monophyletic grouping of the Lokiarchaeota with the eukaryotes. The analysis revealed several genes with cell membrane-related functions. The presence of such genes support the hypothesis of an archaeal host for the emergence of the eukaryotes; the eocyte-like scenarios.

<span class="mw-page-title-main">Parvarchaeota</span> Phylum of archaea

Parvarchaeota is a phylum of archaea belonging to the DPANN archaea. They have been discovered in acid mine drainage waters and later in marine sediments. The cells of these organisms are extremely small consistent with small genomes. Metagenomic techniques allow obtaining genomic sequences from non-cultured organisms, which were applied to determine this phylum.

Hadesarchaea, formerly called the South-African Gold Mine Miscellaneous Euryarchaeal Group, are a class of thermophile microorganisms that have been found in deep mines, hot springs, marine sediments, and other subterranean environments.

Nitrososphaera gargensis is a non-pathogenic, small coccus measuring 0.9 ± 0.3 μm in diameter. N. gargensis is observed in small abnormal cocci groupings and uses its archaella to move via chemotaxis. Being an Archaeon, Nitrososphaera gargensis has a cell membrane composed of crenarchaeol, its isomer, and a distinct glycerol dialkyl glycerol tetraether (GDGT), which is significant in identifying ammonia-oxidizing archaea (AOA). The organism plays a role in influencing ocean communities and food production.

<span class="mw-page-title-main">DPANN</span> A superphylum of Archaea grouping taxa that display various environmental and metabolic features

DPANN is a superphylum of Archaea first proposed in 2013. Many members show novel signs of horizontal gene transfer from other domains of life. They are known as nanoarchaea or ultra-small archaea due to their smaller size (nanometric) compared to other archaea.

"Candidatus Thorarchaeota", or simply Thorarchaeota, is a phylum within the superphylum Asgard archaea. The Asgard superphylum represents the closest prokaryotic relatives of eukaryotes. Since there is such a close relation between the two different domains, it provides further evidence to the two-domain tree of life theory which states that eukaryotes branched from the archaeal domain. Asgard archaea are single cell marine microbes that contain branch like appendages and have genes that are similar to eukarya. The asgard archaea superphylum is composed of Thorarchaeota, Lokiarchaeota, Odinarchaeota, and Heimdallarchaeota. Thorarchaeota were first identified from the sulfate-methane transition zone in tidewater sediments. Thorarcheota are widely distributed in marine and freshwater sediments.

Nikos Kyrpides is a Greek-American bioscientist who has worked on the origins of life, information processing, bioinformatics, microbiology, metagenomics and microbiome data science. He is a senior staff scientist at the Berkeley National Laboratory, head of the Prokaryote Super Program and leads the Microbiome Data Science program at the US Department of Energy Joint Genome Institute.

TM7x, also known as Nanosynbacter lyticus type strain TM7x HMT 952. is a phylotype of one of the most enigmatic phyla, Candidatus Saccharibacteria, formerly candidate phylum TM7. It is the only member of the candidate phylum that has been cultivated successfully from the human oral cavity, and stably maintained in vitro. and serves as a crucial paradigm. of the newly described Candidate Phyla Radiation (CPR). The cultivated oral taxon is designated as Saccharibacteria oral taxon TM7x. TM7x has a unique lifestyle in comparison to other bacteria that are associated with humans. It is an obligate epibiont parasite, or an "epiparasite", growing on the surface of its host bacterial species Actinomyces odontolyticus subspecies actinosynbacter strain XH001, which is referred to as the "basibiont". Actinomyces species are one of the early microbial colonizers in the oral cavity. Together, they exhibit parasitic epibiont symbiosis.

Modulibacteria(Moduliflexota) is a bacterial phylum formerly known as KS3B3 or GN06. It is a candidate phylum, meaning there are no cultured representatives of this group. Members of the Modulibacteria phylum are known to cause fatal filament overgrowth (bulking) in high-rate industrial anaerobic wastewater treatment bioreactors.

References

  1. ↑ Baker, Brett J.; et al. (2006). "Lineages of Acidophilic Archaea Revealed by Community Genomic Analysis". Science . 314 (5807): 1933–1935. Bibcode:2006Sci...314.1933B. doi:10.1126/science.1132690. PMID   17185602. S2CID   26033384.
  2. ↑ Rinke, C; Schwientek, P; Sczyrba, A; Ivanova, NN; Anderson, IJ; Cheng, JF; Darling, A; Malfatti, S; Swan, BK; Gies, EA; Dodsworth, JA; Hedlund, BP; Tsiamis, G; Sievert, SM; Liu, WT; Eisen, JA; Hallam, SJ; Kyrpides, NC; Stepanauskas, R; Rubin, EM; Hugenholtz, P; Woyke, T (2013). "Insights into the phylogeny and coding potential of microbial dark matter". Nature. 499 (7459): 431–437. Bibcode:2013Natur.499..431R. doi: 10.1038/nature12352 . hdl: 1912/6194 . PMID   23851394.
  3. ↑ Castelle, CJ; Wrighton, KC; Thomas, BC; Hug, LA; Brown, CT; Wilkins, MJ; Frischkorn, KR; Tringe, SG; Singh, A; Markillie, LM; Taylor, RC; Williams, KH; Banfield, JF (2015). "Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling". Current Biology. 25 (6): 690–701. doi: 10.1016/j.cub.2015.01.014 . PMID   25702576.
  4. ↑ Juottonen et al. Seasonality of rDNA- and rRNA-derived archaeal communities and methanogenic potential in a boreal mire, ISME Journal 24 July 2008
  5. ↑ Amaral-Zettler et al. Microbial community structure across the tree of life in the extreme Río Tinto, ISME Journal 2010
  6. ↑ Murakami et al. Metatranscriptomic analysis of microbes in an ocean-front deep subsurface hot spring reveals novel small RNAs and type-specific tRNA degradation, Appl Environ Microbiol 2011
  7. ↑ LR Comolli; KH Downing; BJ Baker; CE Siegerist; JF Banfield (2009). "Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon". ISME Journal. 3 (2): 159–167. doi: 10.1038/ismej.2008.99 . PMID   18946497.
  8. 1 2 3 Baker; et al. (2010). "Enigmatic, ultrasmall, uncultivated Archaea". Proc. Natl. Acad. Sci. 107 (19): 8806–8811. Bibcode:2010PNAS..107.8806B. doi: 10.1073/pnas.0914470107 . PMC   2889320 . PMID   20421484.
  9. ↑ Sanders, Robert (3 May 2010). "Weird, ultra-small microbes turn up in acidic mine drainage".
  10. ↑ "Our Projects".
  11. ↑ Dick et al. Community-wide analysis of microbial genome sequence signatures. Archived 2014-07-15 at the Wayback Machine Genome Biology 10:R85
  12. ↑ Fujishima; et al. (2011). "A novel three-unit tRNA splicing endonuclease found in ultrasmall Archaea possesses broad substrate specificity". Nucleic Acids Res. 39 (22): 9695–704. doi:10.1093/nar/gkr692. PMC   3239211 . PMID   21880595.
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