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Spotlight on the Thaumarchaeota The ISME Journal (2012) 6, 227–230 & 2012 International Society for Microbial Ecology All rights reserved 1751-7362/12 www.nature.com/ismej COMMENTARY Spotlight on the Thaumarchaeota C Brochier-Armanet, S Gribaldo and P Forterre The ISME Journal (2012) 6, 227–230; doi:10.1038/ismej. In fact, many lineages of uncultivated archaea have 2011.145; published online 10 November 2011 been reported based on 16S rRNA sequences (Prosser and Nicol, 2008), some of them belonging to the Thaumarchaeota (for example, group I.1c, 1A/ pSL12, ThAOA/HWCG III, SAGMCG-I, SCG and Over the last two decades, many new groups of FSCG, etc.) (Pester et al., 2011). However, the deeply branching uncultivated archaea have been situation is less clear for a few other uncultivated unveiled by molecular screening of 16S rRNA lineages (for example, HWCG I, Miscellaneous genes. Among these, Thaumarchaeota (Brochier- Crenarchaeotic Group, Marine Benthic Group B) Armanet et al., 2008) are now known to represent whose position is unresolved in rRNA phylogenies. a highly diversified and ancient phylum present Regarding HWGC I, Nunoura and coworkers have in a wide variety of ecosystems, including marine recently reconstituted the genome of one of its and fresh waters, soils and also hot environ- members, ‘Ca. Caldiarchaeum subterraneum’, using ments (Pester et al., 2011). The Thaumarchaeota a metagenomic library prepared from a geothermal have rapidly gained much attention after the water stream collected in a subsurface gold discovery that some of them are able to oxidize mine (Nunoura et al., 2011). Based on the ana- ammonia aerobically, providing the first example lysis of the genome sequence, they proposed of nitrification in the Archaea and therefore extend- that ‘Ca. C. subterraneum’ represents a novel ing the range of microorganisms capable of this archaeal phylum, which was tentatively called important metabolism, which was previously ‘Aigarchaeota’. However, in contrast to rRNA trees, thought to be restricted to a few proteobacterial ‘Ca. C. subterraneum’ appears robustly grouped lineages (Konneke et al., 2005). The interest raised with Thaumarchaeota in protein-based phylogenies by Thaumarchaeota is witnessed by the growing (Brochier-Armanet et al., 2011, Nunoura et al., availability over the last 4 years of isolated 2011). This suggests that HWCG I might represent representatives (or enrichment cultures) and of a basal thaumarchaeal lineage, although more data genomic data. This opens up a whole new perspec- from additional representatives is surely necessary tive on the diversity of Archaea and on ancient to clarify the issue. evolution. Further exploration of Thaumarchaeota—including uncultivated subgroups—will be essential to deline- ate more precisely this phylum from a biological, A diverse and ancient phylum ecological and evolutionary point of view. For instance, it will be interesting to know if crenarch- Isolates or enrichment cultures from groups I.1a aeol, a specific lipid identified in the membranes of (Cenarchaeum symbiosium and Nitrosopumilus various Thaumarchaeota and recently proposed to maritimus), I.1b (‘Ca. Nitrososphaera viennensis’) be renamed thaumarchaeol (Pester et al., 2011), is a and ThAOA/HWCG III (‘Ca. Nitrosocaldus yellow- specific feature of the whole phylum. Similarly, it stonii’) have now been reported. In addition, will be important to explore all thaumarchaeal complete genome sequences are now available from lineages for the presence of members capable of three Thaumarchaeota belonging to the marine ammonia oxidation. Indeed, it is possible that not all group I.1a (C. symbiosium, N. maritimus and Thaumarchaeota are ammonia oxidizers, and a key ‘Candidatus (Ca.) Nitrosoarchaeum limnia’), and question will be to understand whether this partial genome data has been released from a important metabolism is ancestral in the phylum, moderately thermophilic strain from soil, ‘Ca. or rather appeared later during its diversification. Nitrososphaera gargensis’ (group I.1b) (see Brochier- For example, the ‘Ca. C. subterraneum’ composite Armanet et al. (2011) and references therein). genome seems to lack the genes coding for ammo- Importantly, these sequence data have confirmed nia-oxidation enzymes. This might suggest that the genomic features and phylogenetic distinctive- ammonia oxidation appeared in Thaumarchaeota ness of the Thaumarchaeota (Spang et al., 2010). after the divergence of HWCG I, but further data Currently available genomic data are, however, far from additional HWCG I representatives and from from covering the whole diversity of this phylum. other deeply branching uncultivated thaumarchaeal Commentary 228 lineages are required to conclude about this cellular systems, sometimes shared either with important issue. Moreover, the exploration of the Bacteria or Eucarya, appears to be a common feature biology and ecological diversity of Thaumarchaeota in Archaea (Brochier-Armanet et al., 2011). The is expected to continue revealing a high diversity of availability of genomic data from the Thaumarch- cellular forms and lifestyles. For example, marine aeota has allowed making this phenomenon all the giant Thaumarchaeota forming multicellular fila- more evident. For instance, the analysis of thau- ments possibly associated with bacterial ectosym- marchaeal genomes has revealed a unique combina- bionts have been recently reported from sulfide rich tion of features shared either with Crenarchaeota, environments of a mangrove tropical swamp (Muller Euryarchaeota or Korarchaeota (Figure 1). A striking et al., 2010). Finally, the availability of genomic data example is the presence of components of two very from a wide variety of thaumarchaeal lineages will different cell division systems: Cdv, previously provide material for the establishment of a detailed thought to be present only in some Crenarchaeota, classification of Thaumarchaeota, and will help and FtsZ, so far thought to be specific of Euryarch- clarifying their phylogenetic relationships with the aeota and Korarchaeota (see Makarova et al. (2010) other major archaeal phyla. and references therein). A major question to be addressed is how these two cell division systems coexist and function in Thaumarchaeota. Interest- A hot-loving ancestor? ingly, the major partner of FtsZ in Bacteria, MinD, is present in Euryarchaeota (Gerard et al., 1998) The presence of Thaumarchaeota, not only in but not in Thaumarchaeota (unpublished observa- mesophilic but also in thermophilic environments tions), suggesting a different role for FtsZ in (de la Torre et al., 2008), confirms the wide range of these two archaeal phyla. The forthcoming avail- phenotypes present in this phylum. It is worth ability of genomic sequence data from basal un- noting that the deepest thaumarchaeal branches are cultured groups will likely confirm the cellular composed of uncultivated groups from various hot systems in the Archaea. As an example, a eukar- environments (de la Torre et al., 2008). This yotic-like ubiquitin modifier system has been found observation, together with the presence of a in the genome of ‘Ca. C. subterraneum’ that is very reverse gyrase in the genome of Ca. C. subterraneum different from those recently identified in prokar- (Nunoura et al. 2011), suggests that the ancestor of yotes (Nunoura et al., 2011), and a eukaryotic-like Thaumarchaeota and ‘Aigarchaeota’ was at least actin has been discovered in Korarchaeota, some thermophile, and that mesophily in some thau- Crenarchaeota (Makarova et al., 2010) and more marchaeal lineages is a derived character. The recently in ‘Ca. C. subterraneum’ (Brochier-Armanet analysis of environmental sequences from Thau- et al., 2011) (Figure 1). The distribution of these marchaeota indicates that adaptation to mesophily components may result from horizontal gene trans- may have been helped through horizontal gene fers between Archaea and Eucarya, Archaea and transfer from bacteria or from mesophilic archaea Bacteria or among Archaea, but may also represent (Lopez-Garcia et al., 2004). Because secondary ancient traits that were present in the common adaptations to mesophily are also observed in ancestor of Archaea and were subsequently lost in Euryarchaeota, this would be consistent with the different archaeal lineages. Investigating further the hypothesis of multiple independent adaptations to great plasticity of archaeal cellular systems, their mesophily in the Archaea from thermophilic or origin and function, will surely provide important hyperthermophilic ancestors. This scenario is also information on the evolutionary paths and adap- supported by recent inferences of ancestral archaeal tive strategies followed by Archaea along their rRNA and protein sequences (Groussin and Gouy, diversification. 2011). The growing availability of genomic data Besides providing insights into the early evolu- from Thaumarchaeota will now allow studying in a tion of cellular features, the discovery of Thau- more precise way such adaptations from thermo- marchaeota is also crucial for understanding the phily to mesophily, for example, whether they have nature of ancient microbial communities. For followed similar or different evolutionary paths example, bacterial nitrification appears to be a with respect to the Euryarchaeota. recent feature because it is present only in a few late-emerging subgroups of g- and b-proteobacteria (Konneke et al., 2005). Therefore, it is tempting A new perspective on archaeal biology to speculate that the very ancient traces of
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