Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses

Abstract

The Miscellaneous Crenarchaeota group (MCG) Archaea is one of the predominant archaeal groups in anoxic environments and may have significant roles in the global biogeochemical cycles. However, no isolate of MCG has been cultivated or characterized to date. In this study, we investigated the genetic organization, ecophysiological properties and evolutionary relationships of MCG archaea with other archaeal members using metagenome information and the result of gene expression experiments. A comparison of the gene organizations and similarities around the 16S rRNA genes from all available MCG fosmid and cosmid clones revealed no significant synteny among genomic fragments, demonstrating that there are large genetic variations within members of the MCG. Phylogenetic analyses of large-subunit+small-subunit rRNA, concatenated ribosomal protein genes and topoisomerases IB gene (TopoIB) all demonstrate that MCG constituted a sister lineage to the newly proposed archaeal phylum Aigarchaeota and Thaumarchaeota. Genes involved in protocatechuate degradation and chemotaxis were found in a MCG fosmid 75G8 genome fragment, suggesting that this MCG member may have a role in the degradation of aromatic compounds. Moreover, the expression of a putative 4-carboxymuconolactone decarboxylase was observed when the sediment was supplemented with protocatechuate, further supporting the hypothesis that this MCG member degrades aromatic compounds.

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

“…One explanation for this trend, one of the most robust in macroecology (Gaston et al, 2000), is related with the alternative concept of 'jack-of-all-trades is master of all' (Brown, 1984;Gaston et al, 1997;Verberk et al, 2010), in which cosmopolitan species that can tolerate a large spectrum of environmental conditions and use a broad range of resources become locally dominant. This concept seems to characterize very well members of the MCG lineage both in terms of resources (Biddle et al, 2008;Lloyd et al, 2013;Meng et al, 2014) and distribution. The MCG lineage was one of the most frequent archaeal lineage found in the sediment habitat as it occurs in 68% (141 sites) of the 207 sediments analyzed.…”

“…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).…”

“…Accordingly, the MCG lineage comprised 21 clades that grouped sequences from uncultured representatives mainly from marine and freshwater sediments and less frequently from hypersaline environments (see color coding in Figure 3). On the basis of this monophyly and deep branching position in the overall archaeal tree several authors have recently proposed that MCG would be considered as a new archaeal phylum called Bathyarchaeota (Rinke et al, 2013, Meng et al, 2014.…”

“…Indeed, members of the MCG are very divergent (up to 24%, based on 16S rRNA gene identity, Kubo et al, 2012) and the whole lineage has been proposed as a new archaeal phylum named Bathyarchaeota (Meng et al, 2014). Although a comprehensive phylogeny subdividing the MCG lineage into 17 monophyletic subgroups has recently been reported (Kubo et al, 2012), many questions remain unanswered concerning the distribution and functions of these subgroups in the different habitats.…”

“…Recent findings from metagenomic data (Meng et al, 2014) and single-cell genomics (Lloyd et al, 2013) provided indirect evidence that members of the MCG lineage may be involved in the degradation of aromatic compounds (for example, protocatechuate) and detrital proteins, respectively. This heterogeneity in the potential substrates used by MCG archaea reflects the extremely high genomic diversity of the lineage (Meng et al, 2014), hindering a full understanding on the ecological role and influence of MCG in biogeochemical cycles.…”