A catalogue of 1,167 genomes from the human gut archaeome

The human gut microbiome plays an important role in health, but its archaeal diversity remains largely unexplored. In the present study, we report the analysis of 1,167 nonredundant archaeal genomes (608 high-quality genomes) recovered from human gastrointestinal tract, sampled across 24 countries and rural and urban populations. We identified previously undescribed taxa including 3 genera, 15 species and 52 strains. Based on distinct genomic features, we justify the split of the Methanobrevibacter smithii clade into two separate species, with one represented by the previously undescribed ‘CandidatusMethanobrevibacter intestini’. Patterns derived from 28,581 protein clusters showed significant associations with sociodemographic characteristics such as age groups and lifestyle. We additionally show that archaea are characterized by specific genomic and functional adaptations to the host and carry a complex virome. Our work expands our current understanding of the human archaeome and provides a large genome catalogue for future analyses to decipher its impact on human physiology.

Vertebrate host phylogeny influences gut archaeal diversity

Commonly used 16S rRNA gene primers do not detect the full range of archaeal diversity present in the vertebrate gut. As a result, several questions regarding the archaeal component of the gut microbiota remain, including which Archaea are host-associated, the specificities of such associations and the major factors influencing archaeal diversity. Using 16S rRNA gene amplicon sequencing with primers that specifically target Archaea, we obtained sufficient sequence data from 185 gastrointestinal samples collected from 110 vertebrate species that span five taxonomic classes (Mammalia, Aves, Reptilia, Amphibia and Actinopterygii), of which the majority were wild. We provide evidence for previously undescribed Archaea–host associations, including Bathyarchaeia and Methanothermobacter, the latter of which was prevalent among Aves and relatively abundant in species with higher body temperatures, although this association could not be decoupled from host phylogeny. Host phylogeny explained archaeal diversity more strongly than diet, while specific taxa were associated with both factors, and cophylogeny was significant and strongest for mammalian herbivores. Methanobacteria was the only class predicted to be present in the last common ancestors of mammals and all host species. Further analysis indicated that Archaea–Bacteria interactions have a limited effect on archaeal diversity. These findings expand our current understanding of Archaea–vertebrate associations.

GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy

The Genome Taxonomy Database (GTDB; https://gtdb.ecogenomic.org) provides a phylogenetically consistent and rank normalized genome-based taxonomy for prokaryotic genomes sourced from the NCBI Assembly database. GTDB R06-RS202 spans 254 090 bacterial and 4316 archaeal genomes, a 270% increase since the introduction of the GTDB in November, 2017. These genomes are organized into 45 555 bacterial and 2339 archaeal species clusters which is a 200% increase since the integration of species clusters into the GTDB in June, 2019. Here, we explore prokaryotic diversity from the perspective of the GTDB and highlight the importance of metagenome-assembled genomes in expanding available genomic representation. We also discuss improvements to the GTDB website which allow tracking of taxonomic changes, easy assessment of genome assembly quality, and identification of genomes assembled from type material or used as species representatives. Methodological updates and policy changes made since the inception of the GTDB are then described along with the procedure used to update species clusters in the GTDB. We conclude with a discussion on the use of average nucleotide identities as a pragmatic approach for delineating prokaryotic species.

Expanding Archaeal Diversity and Phylogeny: Past, Present, and Future

The discovery of the Archaea is a major scientific hallmark of the twentieth century. Since then, important features of their cell biology, physiology, ecology, and diversity have been revealed. Over the course of some 40 years, the diversity of known archaea has expanded from 2 to about 30 phyla comprising over 20,000 species. Most of this archaeal diversity has been revealed by environmental 16S rRNA amplicon sequencing surveys using a broad range of universal and targeted primers. Of the few primers that target a large fraction of known archaeal diversity, all display a bias against recently discovered lineages, which limits studies aiming to survey overall archaeal diversity. Induced by genomic exploration of archaeal diversity, and improved phylogenomics approaches, archaeal taxonomic classification has been frequently revised. Due to computational limitations and continued discovery of new lineages, a stable archaeal phylogeny is not yet within reach. Obtaining phylogenetic and taxonomic consensus of archaea should be a high priority for the archaeal research community. Expected final online publication date for the Annual Review of Microbiology, Volume 75 is October 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Archaea: A Gold Mine for Topoisomerase Diversity

The control of DNA topology is a prerequisite for all the DNA transactions such as DNA replication, repair, recombination, and transcription. This global control is carried out by essential enzymes, named DNA-topoisomerases, that are mandatory for the genome stability. Since many decades, the Archaea provide a significant panel of new types of topoisomerases such as the reverse gyrase, the type IIB or the type IC. These more or less recent discoveries largely contributed to change the understanding of the role of the DNA topoisomerases in all the living world. Despite their very different life styles, Archaea share a quasi-homogeneous set of DNA-topoisomerases, except thermophilic organisms that possess at least one reverse gyrase that is considered a marker of the thermophily. Here, we discuss the effect of the life style of Archaea on DNA structure and topology and then we review the content of these essential enzymes within all the archaeal diversity based on complete sequenced genomes available. Finally, we discuss their roles, in particular in the processes involved in both the archaeal adaptation and the preservation of the genome stability.

Spatiotemporal organization of bacteria/archaea in maize rhizosphere

<p>Plants interact with the rhizosphere microbiome via root exudates that consist of numerous metabolites serving as energy or carbon sources for microbial growth and as modulators of the uncountable rhizosphere interactions. The rhizosphere microbiome plays also an important role in plant health, growth, and productivity. Different drivers are known to shape the rhizosphere microbiome, but limited investigation exists whether there is a spatial variability in the microbiome along the root system (depth). The present study aimed to assess effects of potentially different drivers such as soil substrates, soil compartments (rhizosphere, and bulk soil), depths, and plant genotypes on bacterial/archaeal communities associated with two maize genotypes, root hair defective mutant (rth3), and the corresponding wild-type (WT). Experiments using maize genotypes rth3 and WT, grown on soil substrates loam, and sand under growth chamber, and field conditions were performed. Under growth camber conditions, the rhizosphere samples were harvested at twenty-two days after sowing the maize seeds from three different soil depths at 4.5 – 6.1 (GD1), 9.0 – 10.6 (GD2), and 13.5 – 15.1 (GD3) cm from soil surface. Under field conditions, analyses were carried out using both rhizosphere, and bulk soil samples taken at three developmental growth stages BBCH14, -19, and -59 of the maize plants; each from two depths at (0 – 20) FD1, and FD2 (20 - 40) cm from soil surface, except the BBCH14 (only samples from D1 were available). Bacterial/archaeal communities were analyzed by MiSeq Illumina sequencing of 16S rRNA gene fragments amplified from total community DNAs.</p><p>Under growth chamber conditions, we observed shifts in bacterial/archaeal diversity of maize rhizosphere at different depths as plant genotype- and soil substrate-dependent effects. Depth-dependent effects of maize rhizosphere (rth3/WT) on bacterial/archaeal compositions displayed high differences between GD1, and the GD3 on both soil substrates. The relative abundances of the bacterial phylum Proteobacteria were significantly higher at GD3 than GD1 for both plant genotypes on sand, but not on loam. Overall, the factor soil substrate was the strongest driver of bacterial/archaeal maize rhizosphere, followed by depth, and maize genotype.</p><p>Under field conditions, depths affected the rhizosphere bacterial/archaeal diversity only at the BBCH59 for WT grown on sand. Lower bacterial/archaeal diversity in soil substrates sand than loam was observed at both FD1 and FD2 in the rhizosphere, but not in bulk soil at all developmental growth stages of maize. The bacterial/archaeal diversity of both maize genotypes was not affected by developmental growth stages of maize on both soil substrates, and soil compartments. Depth gradients of bacterial/archaeal community composition in rhizosphere, and bulk soil displayed at BBCH59 on both soil substrates, and they were relatively higher on sand than loam (rhizosphere). Differences in relative abundances of the bacterial phyla Proteobacteria, and Actinobacteria between soil compartments, developmental growth stages of maize were observed mainly at FD1. Overall, factor soil compartment is the strongest driver of bacterial/archaeal communities followed by soil substrates, developmental growth stages and sampling depths for maize grown under field conditions.</p>

A comprehensive analysis of the global human gut archaeome from a thousand genome catalogue

The human gut microbiome plays an important role in health and disease, but the archaeal diversity therein remains largely unexplored. Here we report the pioneering analysis of 1,167 non-redundant archaeal genomes recovered from human gastrointestinal tract microbiomes across countries and populations. We identified three novel genera and 15 novel species including 52 previously unknown archaeal strains. Based on distinct genomic features, we warrant the split of the Methanobrevibacter smithii clade into two separate species, with one represented by the novel Candidatus M. intestini. Patterns derived from 1.8 million proteins and 28,851 protein clusters coded in these genomes showed a substantial correlation with socio-demographic characteristics such as age and lifestyle. We infer that archaea are actively replicating in the human gastrointestinal tract and are characterized by specific genomic and functional adaptations to the host. We further demonstrate that the human gut archaeome carries a complex virome, with some viral species showing unexpected host flexibility. Our work furthers our current understanding of the human archaeome, and provides a large genome catalogue for future analyses to decipher its role and impact on human physiology.

Strong influence of vertebrate host phylogeny on gut archaeal diversity

Commonly used 16S rRNA gene primers miss much of the archaeal diversity present in the vertebrate gut, leaving open the question of which archaea are host associated, the specificities of such associations, and the major factors influencing archaeal diversity. We applied 16S rRNA amplicon sequencing with Archaea-targeting primers to a dataset of 311 fecal/gut samples spanning 5 taxonomic classes (Mammalia, Aves, Reptilia, Amphibia, and Actinopterygii) and obtained from mainly wild individuals (76% were wild). We obtained sufficient archaeal sequence data from 185 samples comprising 110 species that span all 5 classes. We provide evidence for novel Archaea-host associations, including Bathyarchaeia and Methanothermobacter — the latter of which was prevalent among Aves and enriched in higher body temperatures. Host phylogeny more strongly explained archaeal diversity than diet, while specific taxa were associated with each factor. Co-phylogeny was significant and strongest for mammalian herbivores. Methanobacteria was the only class predicted to be present in the last command ancestors of mammals and all host species. Archaea-Bacteria interactions seem to have a limited effect on archaeal diversity. These findings substantially expand on the paradigm of Archaea-vertebrate associations and the factors that explain those associations.SignificanceArchaea play key roles in the vertebrate gut such as promoting bacterial fermentation via consumption of waste products. Moreover, gut-inhabiting methanogenic Archaea in livestock are a substantial source of greenhouse gas production. Still, much is not known of the archaeal diversity in most vertebrates, especially since 16S rRNA sequence surveys often miss much of the archaeal diversity that is present. By applying Archaea-targeted gut microbiome sequencing to a large collection of diverse vertebrates, we reveal new Archaea-host associations such as a high prevalence of Methanothermobacter in birds. We also show that host evolutionary history explains archaeal diversity better than diet, and certain genera in one particular class of Archaea (Methanobacteria) were likely pervasive in the ancestral vertebrate gut.