The Archaea was recognized as a third domain of life 40 years ago. In this Review, Emeet al. outline a brief history of the changing shape of the tree of life and examine how the recent discovery of diverse archaeal lineages has changed our understanding of the evolutionary relationships between the three domains of life and the origin of the eukaryotic cell.
Archaea and the tree of life
In 1977, Woese and Fox proposed the Archaea as a new domain of life and that the tree of life is divided into three branches — the Eukarya, Bacteria and Archaea. Although a three-domain tree was controversial to some, this study was soon accepted, and is widely regarded as one of the most important discoveries in biology of the past century. To mark 40 years of archaea research, this collection of articles from across the Nature group of journals explores the fundamental biology, evolution, metabolic versatility and ecological impact of archaea, and how the discovery of new species is reshaping the tree of life.
One of the most prominent features of archaea is the extraordinary diversity of their viruses. In this Review, Prangishviliet al. summarize their morphological diversity, the molecular biology of their life cycles and virus–host interactions, and discuss their evolution and their role in the global virosphere.
Archaea are highly diverse microorganisms that inhabit various environments. This evolutionary flexibility and adaptability has been supported by abundant horizontal gene transfer. In this Review, Albers and colleagues discuss the mechanisms and consequences of archaeal DNA transfer.
In this Opinion article, López-Garcíaet al. describe recent archaeal phylogenomic data relating to the massive acquisition of bacterial genes by horizontal gene transfer. They argue that the findings presented suggest that the import of these bacterial genes was crucial for the adaptation of archaea to mesophilic lifestyles.
The archaeal genome is organized by either eukaryotic-like histone proteins or bacterial-like architectural proteins. Dame and colleagues discuss the interplay between chromatin proteins and components of the basal and regulatory transcription machinery, and describe how these factors cooperate in nucleoid structuring and gene regulation.
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
The vast increase in the number of 16S ribosomal RNA gene sequences that are now available has led to an urgent need to implement taxonomic boundaries and classification principles that can apply to both cultured and uncultured microorganisms. In this Analysis article, the authors use 16S rRNA gene sequence identities to propose rational taxonomic boundaries for high taxa of bacteria and archaea and suggest a rationale for the circumscription of uncultured taxa that is compatible with the taxonomy of cultured bacteria and archaea.
Villanuevaet al. analyse the relationship between archaeal membrane lipids and the enzymes that are involved in their biosynthesis and conclude that our current understanding of the archaeal membrane lipid biosynthesis pathway needs some reconsideration. On the basis of amino acid sequence analysis, they present an alternative biosynthetic pathway that involves a 'multiple key, multiple lock' mechanism.
Bernander and Lindås provide an overview of recent studies that have enhanced our understanding of the archaeal cell cycle. They discuss the multiple-origin mode of DNA replication, the archaeal replisome, the identification of a genome segregation machinery, the first cytoskeletal structure and the discovery of a novel cell division system.
N-glycosylation was first reported in archaea almost 40 years ago. However, as Jerry Eichler describes in this Progress article, it is only recently, with the ready availability of archaeal genome sequences and new and improved molecular tools, that we have begun to make major advances in our understanding of this crucial post-translational modification.
The evolution of monoderm and diderm cell envelopes, and thus of Gram-positive and Gram-negative bacteria, is a long-standing question. In this Opinion article, Tocheva, Ortega and Jensen propose, based on recent electron cryotomography data, a new model that places sporulation at the heart of bacterial evolution.
Ever since the discovery in 1977 of a group of microorganisms called the Archaea, researchers have generally assumed that all life on Earth can be arranged into three domains: the Bacteria and Archaea, both lacking nuclei but clearly different from one another, and the eukaryotes, which have nucleated cells. But stimulated by the discovery of lineages of environmental Archaea containing genes previously thought specific to eukaryotes, there has been increasing support for a two-domain model of life, in which the eukaryotes evolved from within the Archaea. In this Review, Martin Embley and colleagues conclude that increasing knowledge of archaeal diversity, together with improvements in reconstructing long-sundered phylogenies, now favour the two-domain view.
This review outlines experimental considerations, advances and challenges in microbial single-cell genome sequencing and discusses the applications and scientific questions that this approach enabled.
News & Comment
This issue marks the 40th anniversary of the publication of the landmark article by Carl Woese and George Fox in which they proposed the Archaea as a third domain of life.
In this Essay, Alberset al. discuss the remarkable achievements of two leaders of the archaeal research field: the late Carl Woese and the late Wolfram Zillig. They highlight how the discoveries of these two researchers have inspired the current and upcoming generations of microbiologists.
This month's Genome Watch highlights how metagenomics is continuing to reveal the diversity of microorganisms in the environment and how it is challenging and expanding our understanding of how life evolved on Earth.
This study provides insights into the archaeal ancestor of eukaryotes and the primal stages of eukaryogenesis.
A new large-scale genomics study reports a vastly expanded tree of life that is based on genomic data from over 3,000 species, including many uncultivated and poorly characterized prokaryotes.
Although the origin of eukaryotic cells from prokaryotic ancestors remains an enigma, it has become clear that the root of eukaryotes lies among a group of prokaryotes known as archaea. The recent identification of newly described archaea belonging to the Asgard superphylum, including Lokiarchaeota and Thorarchaeota, revealed a group of prokaryotes containing many proteins and genetic sequences that are otherwise found only in eukaryotes. Thijs Ettema and colleagues extend the search for eukaryotic roots by describing further additions to the Asgard superphylum: the Odinarchaeota and Heimdallarchaeota. The new Asgard genomes encode homologues of several components of eukaryotic membrane-trafficking machineries, suggesting that the archaeal ancestor of eukaryotes was well equipped to evolve the complex cellular features that are characteristic of eukaryotic cells.
Eukaryotic cells are so very different from prokaryotes that understanding eukaryote origins and ancestry has been a puzzle. Genetic work places archaea closer than bacteria to eukaryotes, but biochemically and morphologically, archaea are closer to bacteria than to eukaryotes. But now Thijs Ettema and colleagues have identified archaea — from a core sample from the Loki's Castle hydrothermal active venting site — that fit the bill as a genomic 'starter-kit' to support the increase in the cellular and genomic complexity that is characteristic of eukaryotes. This novel archaeal group, named Lokiarchaeota, is an immediate sister group of eukaryotes in phylogenetic analyses and has a repertoire of proteins otherwise characteristic of eukaryotes.
Research on the anaerobic oxidation of natural gas has largely been focused on methane as the most abundant constituent. It is less clear how short-chain alkanes—including ethane, propane, n-butane and iso-butane, which together make up about 20% of natural gas—are anaerobically metabolized. Sulfate-reducing bacteria are the only organisms known to date to anaerobically oxidize short-chain hydrocarbons. Gunter Wegener and colleagues identify an anaerobic thermophilic enrichment culture composed of dense consortia of archaea and bacteria that uses a pathway similar to anaerobic methane oxidation, which was previously thought to be specific for C1-compounds, to oxidize butane. Archaea activate butane, and reducing equivalents are channelled to sulfate-reducing partner bacteria. Similar consortia are detected in marine subsurface sediments, suggesting that this pathway may be widespread in nature.
An update to the ‘tree of life’ has revealed a dominance of bacterial diversity in many ecosystems and extensive evolution in some branches of the tree. It also highlights how few organisms we have been able to cultivate for further investigation.
A phylogenetic approach was used to illuminate the physiology of the last universal common ancestor, supporting the theory that LUCA was an H2-dependent autotroph in a hydrothermal setting rich in hydrogen, carbon dioxide and iron.
Diversity-generating retroelements are abundant in the reduced genomes of bacteria and archaea belonging to the CPR and DPANN phyla, driving hypervariability on proteins involved in signalling, transcriptional regulation, attachment and defence.
Significant gaps in our characterization of microbial diversity remain; this meta-analysis of amplicon-based rRNA studies shows that they miss approximately 10% of environmental microbial sequences, most belonging to the candidate phyla radiation.
The recovery of 7,903 bacterial and archaeal metagenome-assembled genomes increases the phylogenetic diversity represented by public genome repositories and provides the first representatives from 20 candidate phyla.
Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis
Methanonatronarchaeia are a distinct class-level lineage of extremely halophilic methanogens, which lack features of classical methanogenesis and have a high intracellular concentration of potassium, suggesting potassium-based osmoprotection.
Genomic reconstruction from hot spring sediment metagenomes show that 'Hadesarchaea' have streamlined yet metabolically versatile genomes, with genes involved in CO and H2 oxidation, with potential coupling to nitrite reduction to ammonia.
Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments
Genetic evidence demonstrates that some Bathyarchaeota lineages are capable of homoacetogenesis, a metabolism so far restricted to the Bacteria.
The Verstraetearchaeota encode divergent methyl-coenzyme M reductase genes, which are required for methylotrophic methanogenesis, increasing methanogen diversity and the complexity of the global methane cycle.
Comparative genomic analyses suggest that Lokiarchaeota, the closest known prokaryotic relative of eukaryotes, are hydrogen dependent, supporting the ‘hydrogen hypothesis’ for the origin of eukaryotic cells.
A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells
An archaeal plasmid that can be transported in membrane vesicles, similar to a virus, and encodes proteins that can insert into host membranes and membrane vesicles, provides insights into the evolutionary link between plasmids and viruses.
Direct observation of rotation and steps of the archaellum in the swimming halophilic archaeon Halobacterium salinarum
3D tracking of quantum dots, cross-kymography and computational modelling reveals a left-hand corkscrew motion of the H. salinarum archaellum, with a right-handed helical structure and a motor efficiency of 6–10%.
CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus
A cryoEM structure of the archaeal flagella, the archaellum, shows distinct features from related bacterial structures.
Termination sequencing reveals that several archaeal genes contain multiple consecutive-terminators, which results in the generation of alternative 3′ UTR isoforms during transcription, similar to what is observed in eukaryotes.
A global analysis of transcription reveals two modes of Spt4/5 recruitment to archaeal RNA polymerase
A transcriptional analysis of Methanocaldococcus jannaschii identifies Spt4/5 as a general elongation factor in Archaea with two modes of recruitment to the RNA polymerase.
Crystal structures of the Argonaute protein from the archaeon Methanocaldococcus jannaschii (MjAgo) in its apo state and bound to a guide DNA elucidate the molecular mechanisms that drive DNA-guided DNA silencing in Archaea.
In addition to canonical guide-dependent endonuclease activity, the Argonaute protein from the archaeon Methanocaldococcus jannaschii (MjAgo) is capable of guide-independent DNA cleavage, enabling MjAgo to process plasmids and genomic DNA.
Metagenomic and microbial sequence data are made easier to interpret with the addition of 1,003 genomes to the Genomic Encyclopedia of Bacteria and Archaea.
Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment
Many microbial lineages have not yet been cultured, which hampers our understanding of their physiology. Here, Wurch et al. use single-cell genomics to infer cultivation conditions for the isolation of a tiny ectosymbiotic nanoarchaeon and its crenarchaeota host from a geothermal spring.
Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea
The contribution of marine archaea to the ocean's carbon cycle is unclear. Here, Li et al. analyse the genomes and transcriptomes from five deep-sea archaeal groups to reveal their metabolic characteristics, suggesting a crucial role in modulating the carbon cycle in deep oceans.
Diversity-generating retroelements (DGRs) are genetic elements that introduce sequence variation within target genes in bacteria and their viruses. Here, Paul et al. report the discovery of DGRs in an archaeal virus and in two archaea from marine and terrestrial subsurface environments, respectively.
Although not photosynthetic, some archaea possess RuBisCO, one of the enzymes characteristic of the photosynthetic Calvin-Benson cycle, but apparently lack another one, phosphoribulokinase (PRK). Here the authors describe a carbon metabolic pathway in methanogenic archaea, involving RuBisCO and PRK.
In the absence of complete genomes, the metabolic capabilities of uncultured ARMAN-like archaea have been uncertain. Here, Golyshina et al. apply an enrichment culture technique and find that the ungapped genome of the ARMAN-like archaeon Mia14 has lost key metabolic pathways, suggesting dependence on the host archaeon Cuniculiplasma divulgatum.
Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius
Small archaeal ubiquitin-like modifiers (SAMPs) have been hypothesized to be part of an ancestral version of the ubiquitin-proteasome system. Here, Anjum et al. identify a SAMP homologous to the eukaryotic ubiquitin-related modifier-1 and show that it is processed by the 20S core proteasome in S. acidocaldarius.
The Critical Assessment of Metagenome Interpretation (CAMI) community initiative presents results from its first challenge, a rigorous benchmarking of software for metagenome assembly, binning and taxonomic profiling.