Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling

Castelle, Cindy J.; Wrighton, Kelly; Thomas, Brian C.; Hug, Laura; Brown, Christopher T.; Wilkins, Michael J.; Frischkorn, Kyle R.; Tringe, Susannah G.; Singh, Anil K.; Markillie, Lye Meng; Taylor, Ron; Williams, Kenneth H.; Banfield, Jillian F.

doi:10.1016/j.cub.2015.01.014

Cited by 501 publications

(660 citation statements)

References 60 publications

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“…These include elucidation of several phyla previously lacking genomic representatives [27][28][29] , including the Patescibacteria superphylum 4 , which has subsequently been referred to as the 'Candidate Phyla Radiation' (CPR) as it may consist of upwards of 35 candidate phyla 10,30 . Notable evolutionary and metabolic insights include the discovery of eukaryotic-like cytoskeleton genes in the archaeon Lokiarchaeota 31,32 and the identification of putative methane-metabolizing genes in the Bathyarchaeota and Verstraetearchaeota phyla 33,34 .…”

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confidence: 99%

Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life

et al. 2017

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Challenges in cultivating microorganisms have limited the phylogenetic diversity of currently available microbial genomes. This is being addressed by advances in sequencing throughput and computational techniques that allow for the cultivation-independent recovery of genomes from metagenomes. Here, we report the reconstruction of 7,903 bacterial and archaeal genomes from > 1,500 public metagenomes. All genomes are estimated to be ≥ 50% complete and nearly half are ≥ 90% complete with ≤ 5% contamination. These genomes increase the phylogenetic diversity of bacterial and archaeal genome trees by > 30% and provide the first representatives of 17 bacterial and three archaeal candidate phyla. We also recovered 245 genomes from the Patescibacteria superphylum (also known as the Candidate Phyla Radiation) and find that the relative diversity of this group varies substantially with different protein marker sets. The scale and quality of this data set demonstrate that recovering genomes from metagenomes provides an expedient path forward to exploring microbial dark matter. Articles NATuRe MiCRobiologyform the UBA data set as they met our filtering criteria of having an estimated quality ≥ 50 (defined as the estimated completeness of a genome minus five times its estimated contamination) and consisting of ≤ 500 scaffolds with an N50 ≥ 10 kb ( Fig. 1 and Supplementary Table 2). Over 93% of the 7,903 UBA genomes have an average coverage of ≥ 10× (5th percentile, 9.2× , 95th percentile, 268× ) and 95.8% have > 5× coverage over 90% of bases, providing assurance of high-quality base-calling across the genomes 3,36 . Among the UBA genomes is a subset of 3,438 near-complete genomes (3,225 bacterial and 213 archaeal) estimated to be ≥ 90% complete with ≤ 5% contamination (Fig. 1a). These genomes consist of ≤ 100 scaffolds in 70.2% of cases (≤ 200 scaffolds in 92.0% genomes) and have an average N50 of 136 kb. Comparison of near-complete UBA genomes that are conspecific strains of complete isolate genomes also suggest that the recovered MAGs have no systematic loss of genomic content, with the exception of extrachromosomal elements such as plasmids (Supplementary Note 1).The UBA data set was also assessed relative to the criteria used by the Human Microbiome Project (HMP) for defining high-quality draft genomes 3,37 . Of the 3,438 UBA genomes we have defined as near complete, 3,201 (93.1%) pass all of the HMP criteria, with the only substantial exception being 4.8% of the genomes having scaffolds with an N50 of < 20 kb (Supplementary Table 3). Nearly half of the remaining 4,465 UBA genomes also pass the HMP criteria for being high quality except that they are estimated to be < 90% complete.The presence of tRNAs for the standard 20 amino acids was examined as a secondary measure of genome quality (Fig. 1c). The 3,438 near-complete UBA genomes have tRNAs that encode for an average of 17.3 ± 2.2 of the 20 amino acids and ≥ 15 amino acids in 90.3% of the genomes. The correlation between estimated genome completeness and identified tRN...

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Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life

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“…Many of the DPANN Archaea described to date have small cells (<1 μm) (5) and reduced genomes in which many core metabolic pathways are incomplete (5). The first DPANN to be characterized, Nanoarchaeum equitans, is obligately dependent on the crenarchaeote Ignicoccus hospitalis for growth (33), and other members of the group also have been observed in direct contact with larger archaeal cells (34), suggesting that symbiotic or parasitic lifestyles may be a common feature of the DPANN lineage.…”

Section: Resultsmentioning

confidence: 99%

“…In addition to the classically defined Euryarchaeota and Crenarchaeota (1), the scope of archaeal diversity has been dramatically expanded in recent years by the discovery of major new lineages using traditional and molecular methods. These lineages are of major ecological and evolutionary significance and include the Thaumarchaeota (2, 3), ammonia oxidizers found in soils and the open ocean, where they play a critical role in the global nitrogen cycle (3); the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaea) Archaea, a diverse group with small cells and genomes, whose reduced metabolic repertoires suggest that they may be symbionts or parasites of other prokaryotes (4,5); and the "Asgard" Archaea, the closest archaeal relatives of eukaryotes described to date (6,7), whose phylogenetic position and gene content are key to ongoing debates about eukaryote origins. In recent years, phylogenetic analyses have supported a clade uniting the Thaumarchaeota, Crenarchaeota, Aigarchaeota, and Korarchaeota that has been informally named the "TACK" Archaea (8) or "Proteoarchaeota" (9).…”

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Integrative modeling of gene and genome evolution roots the archaeal tree of life

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et al. 2017

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

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A root for the archaeal tree is essential for reconstructing the metabolism and ecology of early cells and for testing hypotheses that propose that the eukaryotic nuclear lineage originated from within the Archaea; however, published studies based on outgroup rooting disagree regarding the position of the archaeal root. Here we constructed a consensus unrooted archaeal topology using protein concatenation and a multigene supertree method based on 3,242 single gene trees, and then rooted this tree using a recently developed model of genome evolution. This model uses evidence from gene duplications, horizontal transfers, and gene losses contained in 31,236 archaeal gene families to identify the most likely root for the tree. Our analyses support the monophyly of DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaea), a recently discovered cosmopolitan and genetically diverse lineage, and, in contrast to previous work, place the tree root between DPANN and all other Archaea. The sister group to DPANN comprises the Euryarchaeota and the TACK Archaea, including Lokiarchaeum, which our analyses suggest are monophyletic sister lineages. Metabolic reconstructions on the rooted tree suggest that early Archaea were anaerobes that may have had the ability to reduce CO 2 to acetate via the Wood-Ljungdahl pathway. In contrast to proposals suggesting that genome reduction has been the predominant mode of archaeal evolution, our analyses infer a relatively small-genomed archaeal ancestor that subsequently increased in complexity via gene duplication and horizontal gene transfer.evolution | phylogenetics | Archaea

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“…The latter archaeal group, the seventh order of methanogens, are methylotrophic methanogens obtaining energy and carbon from methanol and methylated amines (Paul et al, 2012;Dridi et al, 2012;Iino et al, 2013;Borrel et al, 2014). Although no information on the potential metabolism of the Terrestrial Miscellaneous Euryarchaeotal Group group is available, recent findings from metagenomic data (Meng et al, 2014;Castelle et al, 2015) and single-cell genomics (Lloyd et al, 2013) suggested that members of the MCG and Marine Benthic Group D lineages may be involved in the degradation of detrital proteins both in marine and continental sediments. The high PD of the MCG lineage invalidates any general assumption of potential metabolisms shared between all MCG subgroups (the specialization of certain subgroups towards freshwater and marine habitats is a good example of this).…”

Section: Evolutionary Relationships Between Freshwater and Marine Mcgmentioning

confidence: 99%

Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage

et al. 2015

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Members of the archaeal Miscellaneous Crenarchaeotic Group (MCG) are among the most successful microorganisms on the planet. During its evolutionary diversification, this very diverse group has managed to cross the saline-freshwater boundary, one of the most important evolutionary barriers structuring microbial communities. However, the current understanding on the ecological significance of MCG in freshwater habitats is scarce and the evolutionary relationships between freshwater and saline MCG remains poorly known. Here, we carried out molecular phylogenies using publicly available 16S rRNA gene sequences from various geographic locations to investigate the distribution of MCG in freshwater and saline sediments and to evaluate the implications of salinefreshwater transitions during the diversification events. Our approach provided a robust ecological framework in which MCG archaea appeared as a core generalist group in the sediment realm. However, the analysis of the complex intragroup phylogeny of the 21 subgroups currently forming the MCG lineage revealed that distinct evolutionary MCG subgroups have arisen in marine and freshwater sediments suggesting the occurrence of adaptive evolution specific to each habitat. The ancestral state reconstruction analysis indicated that this segregation was mainly due to the occurrence of a few saline-freshwater transition events during the MCG diversification. In addition, a network analysis showed that both saline and freshwater MCG recurrently co-occur with archaea of the class Thermoplasmata in sediment ecosystems, suggesting a potentially relevant trophic connection between the two clades.

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Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling

Cited by 501 publications

References 60 publications

Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life

Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life

Integrative modeling of gene and genome evolution roots the archaeal tree of life

Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage

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