Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life

BACKGROUND

Archaea have been recognized as a major domain of life besides Bacteria and Eukarya for about 40 years. Much of the pioneering research on archaeal organisms was dedicated to studying cellular machineries governing basal cellular processes such as transcription and translation and on elucidating physiological characteristics of the few archaeal strains that could be cultured. Although environmental surveys had started to reveal a plethora of uncultured archaeal lineages during the 1990s, in-depth knowledge about their diversity, ecology, and evolution remained limited. Recent developments in the field of metagenomics and single-cell genomics, however, have allowed the reconstruction of archaeal genomes directly from environmental samples without prior cultivation. Altogether, the use of these cultivation-independent approaches has led to the discovery of a multitude of previously unidentified archaeal lineages, some of which represent completely new branches in the archaeal tree. In this Review, we provide an overview of the currently recognized archaeal diversity, summarize new findings on the metabolic potential of recently described archaeal lineages, and discuss these data in light of archaeal evolution.

ADVANCES

Up until about a decade ago, all archaea were assigned to one of two major clades: the Crenarchaeota, which mostly comprise extreme thermophiles, or the Euryarchaeota, which mainly included methanogens and halophiles. Since then, our knowledge on archaeal diversity has increased rapidly. Now, Archaea include at least four major supergroups, the Euryarchaeota and the TACK, Asgard, and DPANN archaea, all of which comprise several different, potentially phylum-rank clades (see the figure). The lineages of these groups are not restricted to extreme habitats, as was once thought common for archaeal species; rather, archaea are widespread and occur in all thinkable environments on Earth, where they can make up substantial portions of the microbial biomass.

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In line with their vast diversity, comparative genomics analyses reveal that Archaea are metabolically versatile and are characterized by different lifestyles. Recently discovered archaeal lineages include mesophiles and (hyper-)thermophiles, anaerobes and aerobes, autotrophs and heterotrophs, a large diversity of putative archaeal symbionts, as well as previously unknown acetogens and different groups of methanogens (see the figure). In fact, both the genetic potential to use the ancient Wood-Ljungdahl carbon fixation pathway and indications for methanogenic traits as well as the ability to anaerobically oxidize methane and other short hydrocarbons have now been found in various lineages outside the Euryarchaeota—the phylum comprising traditional methanogens and methane oxidizers. So far, little is known about the actual physiology of these archaea in their environmental niches or about their potential syntrophic relationships with other organisms, but recent findings highlight the importance and wide occurrence of these metabolic regimes in a wide diversity of archaea from anaerobic environments. Furthermore, these findings support hypotheses that suggest that all extant archaea evolved from an anaerobic autotrophic ancestor that used the Wood-Ljungdahl pathway and may have been able to obtain energy through methanogenesis.

Last, the investigation of informational processing and cellular machineries have revealed that genomes of Asgard archaea, which affiliate with eukaryotes in the tree of life (see the figure), encode proteins that they only share with eukaryotes. Excitingly, these proteins are functionally enriched for membrane bending, vesicular biogenesis, and trafficking activities, suggesting that eukaryotes evolved from an archaeal host that contained some key components that governed the emergence of eukaryotic cellular complexity after endosymbiosis. It will be exciting to determine the function of these proteins, which may be involved in species-species interactions in extant members of the Asgard archaea.

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OUTLOOK

The wealth of novel archaeal genomic data represents a treasure trove for generating testable hypotheses on the metabolic and cellular features of these archaea and will thus help to unveil their thus far poorly characterized biology. Recent findings emphasize the importance of investigating members of the archaeal domain of life in order to obtain a more comprehensive view of microbial ecology, symbiosis, and metabolic interdependencies involving archaeal partners, and of evolution of life on Earth in regard to the deep roots of archaea as well as our microbial ancestry.

The archaeal tree of life.

Schematic phylogenetic tree including major archaeal groups for which genomic data are currently available. The currently recognized groups include the Euryarchaeota (green branches) and the TACK, Asgard, and DPANN archaea (tan, yellow, and pink branches, respectively). Eukaryotes (gray branch) are suggested to have emerged from the Asgard archaea upon endosymbiosis with an alphaproteobacterial partner (the mitochondrial endosymbiont). For each archaeal lineage, key characteristics regarding metabolism and lifestyle are depicted.

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