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  • Review Article
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Genomic studies of uncultivated archaea

Key Points

  • Members of the domain Archaea are diverse and widespread, being found not only in extreme environments, such as hot springs and deep-sea hydrothermal vents, but also in a range of moderate and aerobic environments, such as marine and freshwater plankton, as well as soils.

  • Although the distribution and abundance of archaea in soils, oceans and marine sediments implies that they contribute to global energy cycles, no representatives from these environments have been cultivated in the laboratory, and their specific metabolisms therefore remain elusive. However, the recent advances in environmental genomic studies (the subject of this Focus issue) mean that we can now characterize these organisms using cultivation-independent methods, and form hypotheses about the specific metabolism of several novel archaeal groups.

  • Some of the key findings from the first environmental genomic studies of Archaea are discussed, including the first clues regarding the energy metabolism of crenarchaeota in soil and marine environments that might be capable of ammonia oxidation, the discovery of the crenarchaote–metazoan symbiosis between Cenarchaeum symbiosum and a marine sponge, and the modelling of reverse methanogenesis of methane-oxidizing euryarchaeota. Furthermore, the reconstruction of a mosaic genome for a Ferroplasma species from an environmental dataset is presented. Together with other studies, it shows an unexpected degree of microheterogeneity and genome dynamics.

  • The results obtained from the first environmental genomic datasets are extremely encouraging, as they open up a number of novel hypotheses on the physiology and ecology of archaea. Furthermore, they provide insight into population structures and speciation, which cannot be obtained in this depth through the analysis of laboratory strains. But several challenges must be overcome if the full potential of cultivation-independent analyses is to be met. Novel, even more efficient cloning and sequencing technologies are needed if attempts to analyse the complete genomes of the most abundant species of complex microbial environments are to be successful. However, specific microbial lineages might be targeted in the future, using a second generation of metagenomic technologies that allow an a priori enrichment for specific genomes.

  • Whereas traditional cultivation efforts to isolate novel species will remain important for our understanding of the physiological diversity of microorganisms, it has become clear that environmental genomics marks an important and crucial area in microbiology that will allow us to understand or at least approach the existing diversity and ecological impact of archaea (and bacteria) on this planet, as well as their interaction with other life forms.

Abstract

Archaea represent a considerable fraction of the prokaryotic world in marine and terrestrial ecosystems, indicating that organisms from this domain might have a large impact on global energy cycles. However, many novel archaeal lineages that have been detected by molecular phylogenetic approaches have remained elusive because no laboratory-cultivated strains are available. Environmental genomic analyses have recently provided clues about the potential metabolic strategies of several of the uncultivated and abundant archaeal species, including non-thermophilic terrestrial and marine crenarchaeota and methanotrophic euryarchaeota. These initial studies of natural archaeal populations also revealed an unexpected degree of genomic variation that indicates considerable heterogeneity among archaeal strains. Here, we review genomic studies of uncultivated archaea within a framework of the phylogenetic diversity and ecological distribution of this domain.

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Figure 1: The domain Archaea — from diversity to function.
Figure 2: Visualization of uncultivated archaea in various environments by fluorescence in situ hybridization (FISH).
Figure 3: Conservation among genomic regions of uncultivated marine crenarchaeota.
Figure 4: Expansion of the Amo/Pmo protein family by environmental genomic sequencing — hints of ammonia oxidation in moderate Crenarchaeota.

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Acknowledgements

We dedicate this article to Wolfram Zillig, a pioneer in archaeal research and good friend, who died April 23, 2005 in Munich. Thanks to H.-P. Klenk for the amoA tree, to A. Treusch, S. Leininger and S. Schuster for work on soil clone 54d9, to A. Kletzin and S. Norland for bioinformatic support and to V. Torsvik and colleagues (University of Bergen) for fruitful discussions. Special thanks from C.S. to E.F. DeLong for continuous encouragement since the first days of environmental genomics. The work in C.S.'s laboratory is supported by the Bundesministerium für Bildung und Forschung, the EMBO Young Investigator Programme and the University of Bergen.

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DEEP SUBSURFACE

Usually 50 m or more below the surface, where the microbiota is not immediately affected by microbial functions or biogeochemical processes of the surface (as opposed to shallow subsurface).

BENTHIC

Living in or on the bottom of a body of water.

SYNTENIC

Relationship between chromosomal regions of different species where homologous genes occur in the same order.

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Schleper, C., Jurgens, G. & Jonuscheit, M. Genomic studies of uncultivated archaea. Nat Rev Microbiol 3, 479–488 (2005). https://doi.org/10.1038/nrmicro1159

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