Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon

Comolli, Luis R.; Baker, Brett J.; Downing, Kenneth H.; Siegerist, Cristina; Banfield, Jillian F.

doi:10.1038/ismej.2008.99

Cited by 113 publications

(122 citation statements)

References 32 publications

Supporting

Mentioning

117

Contrasting

Order By: Relevance

“…Nano-sized archaea were first described from hot springs environments (Huber et al, 2002), then in acid mine drainage (Baker and Banfield, 2003;Comolli et al, 2009) and subsequently in hypersaline environments (Narasingarao et al, 2012). More recently, single cell sequencing results suggested the existence of other clades of nano-sized archaea (Rinke et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…More recently, single cell sequencing results suggested the existence of other clades of nano-sized archaea (Rinke et al, 2013). There is genomic and physical evidence that both the hyperthermophile Nanoarchaeum equitans and the acidophilic ARMAN lineage organisms depend on an associated organism for many metabolic needs (Huber et al, 2002;Comolli et al, 2009;Podar et al, 2013). Both have been co-cultivated with other organisms (Igniococcus in the case of Nanoarchaeum equitans; biofilm communities in the case of ARMAN).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

et al. 2015

Self Cite

View full text Add to dashboard Cite

Marine microbial communities experience daily fluctuations in light and temperature that can have important ramifications for carbon and nutrient cycling. Elucidation of such short time scale community-wide dynamics is hindered by system complexity. Hypersaline aquatic environments have lower species richness than marine environments and can be well-defined spatially, hence they provide a model system for diel cycle analysis. We conducted a 3-day time series experiment in a well-defined pool in hypersaline Lake Tyrrell, Australia. Microbial communities were tracked by combining cultivation-independent lipidomic, metagenomic and microscopy methods. The ratio of total bacterial to archaeal core lipids in the planktonic community increased by up to 58% during daylight hours and decreased by up to 32% overnight. However, total organism abundances remained relatively consistent over 3 days. Metagenomic analysis of the planktonic community composition, resolved at the genome level, showed dominance by Haloquadratum species and six uncultured members of the Halobacteriaceae. The post 0.8 μm filtrate contained six different nanohaloarchaeal types, three of which have not been identified previously, and cryo-transmission electron microscopy imaging confirmed the presence of small cells. Notably, these nano-sized archaea showed a strong diel cycle, with a pronounced increase in relative abundance over the night periods. We detected no eukaryotic algae or other photosynthetic primary producers, suggesting that carbon resources may derive from patchily distributed microbial mats at the sediment-water interface or from surrounding land. Results show the operation of a strong community-level diel cycle, probably driven by interconnected temperature, light abundance, dissolved oxygen concentration and nutrient flux effects.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

et al. 2015

Self Cite

View full text Add to dashboard Cite

show abstract

“…Cryogenic transmission electron microscopy specimen preparation and imaging were done as described by Comolli et al (2009) and Baker et al (2010).…”

Section: Methodsmentioning

confidence: 99%

Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities

et al. 2014

Self Cite

View full text Add to dashboard Cite

A fundamental question in microbial ecology relates to community structure, and how this varies across environment types. It is widely believed that some environments, such as those at very low pH, host simple communities based on the low number of taxa, possibly due to the extreme environmental conditions. However, most analyses of species richness have relied on methods that provide relatively low ribosomal RNA (rRNA) sampling depth. Here we used community transcriptomics to analyze the microbial diversity of natural acid mine drainage biofilms from the Richmond Mine at Iron Mountain, California. Our analyses target deep pools of rRNA gene transcripts recovered from both natural and laboratory-grown biofilms across varying developmental stages. In all, 91.8% of the B254 million Illumina reads mapped to rRNA genes represented in the SILVA database. Up to 159 different taxa, including Bacteria, Archaea and Eukaryotes, were identified. Diversity measures, ordination and hierarchical clustering separate environmental from laboratory-grown biofilms. In part, this is due to the much larger number of rare members in the environmental biofilms. Although Leptospirillum bacteria generally dominate biofilms, we detect a wide variety of other Nitrospira organisms present at very low abundance. Bacteria from the Chloroflexi phylum were also detected. The results indicate that the primary characteristic that has enabled prior extensive cultivation-independent 'omic' analyses is not simplicity but rather the high dominance by a few taxa. We conclude that a much larger variety of organisms than previously thought have adapted to this extreme environment, although only few are selected for at any one time.

show abstract

“…The lineages have been detected in other acidic environments (21,22). ARMAN cells have volumes of 0.009 μm 3 to 0.04 μm 3 , close to the theoretical lower limit for life, and almost all cells contain a mysterious tubular organelle that is roughly 200 nm long and 60 nm wide (23).…”

mentioning

confidence: 95%

“…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).…”

mentioning

confidence: 99%

Enigmatic, ultrasmall, uncultivated Archaea

Baker¹,

Comolli

Dick³

et al. 2010

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

307

296

View full text Add to dashboard Cite

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...

show abstract

Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon

Cited by 113 publications

References 32 publications

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities

Enigmatic, ultrasmall, uncultivated Archaea

Contact Info

Product

Resources

About