Recoding of stop codons expands the metabolic potential of two novel Asgardarchaeota lineages
Year: 2021
Type: article
Abstract: Asgardarchaeota have been proposed as the closest living relatives to eukaryotes, and a total of 72 metagenome-assembled genomes (MAGs) representing six primary lineages in this archaeal phylum have thus far been described. These organisms are predicted to be fermentative heterotrophs contributing to carbon cycling in sediment ecosystems. Here, we double the genomic catalogue of Asgardarchaeota by obtaining 71 MAGs from a range of habitats around the globe, including the deep subsurface, brackish shallow lakes, and geothermal spring sediments. Phylogenomic inferences followed by taxonomic rank normalisation confirmed previously established Asgardarchaeota classes and revealed four additional lineages, two of which were consistently recovered as monophyletic classes. We therefore propose the names Candidatus Sifarchaeia class nov. and Ca. Jordarchaeia class nov., derived from the gods Sif and Jord in Norse mythology. Metabolic inference suggests that both classes represent hetero-organotrophic acetogens, which also have the ability to utilise methyl groups such as methylated amines, with acetate as the probable end product in remnants of a methanogen-derived core metabolism. This inferred mode of energy conservation is predicted to be enhanced by genetic code expansions, i.e., stop codon recoding, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec recoding in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl recoding, on the other hand, is restricted to Sifarchaeia in the Asgardarchaeota, making it the first reported non-methanogenic archaeal lineage with an inferred complete Pyl machinery, likely providing members of this class with an efficient mechanism for methylamine utilisation. Furthermore, we identified enzymes for the biosynthesis of ester-type lipids, characteristic of bacteria and eukaryotes, in both newly described classes, supporting the hypothesis that mixed ether-ester lipids are a shared feature among Asgardarchaeota.
Source: ISME Communications
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: gold
Estimated APC paid: $2,380
Awards: Archaeal dark matter and the origin of eukaryotes, G1286236842, G1414775356, G1632040200, G1816284028, G1863003419, G3083819904, G365575497, G419881185, G4206956643, G42916606, Collaborative Proposal: Biodiversity discovery and analysis of "Aigarchaeota", a globally distributed but poorly understood archaeal lineage, G4501827968, G498139845, G5866790777, RECENT ADVANCEMENTS IN METAGENOMICS AND SINGLE-CELL GENOMICS HAVE ENABLED UNPRECEDENTED ACCESS TO GENOMES FROM CANDIDATE (YET-UNCULTIVATED) PHYLA OF BACTERIA AND ARCHAEA INCLUDING THOSE INHABITING EXTREME AND EARLY EARTH-LIKE SYSTEMS. THESE DATA HAVE ENABLED INSIGHTS INTO THE BIOLOGY OF THESE ORGANISMS INCLUDING THEIR CATABOLIC AND ANABOLIC POTENTIAL MOLECULAR ADAPTATIONS TO LIFE IN EXTREME ENVIRONMENTS AND INSIGHTS INTO THE EARLY DIVERSIFICATION OF MICROBIAL LINEAGES. HOWEVER THE PREDICTED METABOLIC FUNCTIONS OF THESE ORGANISMS AND THEIR GENES REMAIN LARGELY UNTESTED. THE CENTRAL GOAL OF THIS PROPOSAL IS TO LEVERAGE A FOUNDATION OF GENOMIC EXPLORATION IN GREAT BOILING SPRING (GBS) NV TO ASSESS METABOLIC FUNCTIONS OF THERMOPHILES REPRESENTING CANDIDATE PHYLA OF BACTERIA AND ARCHAEA AND THEIR ROLES IN MAJOR BIOGEOCHEMICAL CYCLES. WE HAVE RECENTLY DESCRIBED THE FIRST SUBSTANTIAL GENOMIC DATA FOR THE CANDIDATE BACTERIAL PHYLA ATRIBACTERIA (OP9) CALESCAMANTES (EM19) AND FERVIDIBACTERIA (OCTSPA1-106) AND KRYPTONIA. TO ADDRESS THE METABOLIC FUNCTIONS OF THESE AND OTHER YET-UNCULTIVATED MAJOR LINEAGES WE WILL USE A COMBINATION OF TARGETED AND BROADBASED APPROACHES. OBJECTIVE 1: ASSESS C AND N ASSIMILATORY METABOLISMS IN SPECIFIC TARGETED TAXA IN MICROCOSMS AND ENRICHMENT CULTURES USING (A) STABLE-ISOTOPE PROBING (SIP) FLUORESCENCE IN SITU HYBRIDIZATION AND NANOSIMS IMAGING (FISH-SIMS) AND (B) IN SITU TRANSCRIPTION OF GENES PREDICTED TO BE INVOLVED IN H C N AND S CYCLING BY QUANTITATIVE REVERSE-TRANSCRIPTASE PCR. OBJECTIVE 2: DETERMINE METABOLIC FUNCTION OF ABUNDANT COMMUNITY MEMBERS USING BROAD-BASED APPROACHES SUCH AS (A) 16S RRNA SIP WITH A CUSTOM PHYLOGENETIC MICROARRAY (CHIP-SIP) TO ASSESS C AND N ASSIMILATION IN MICROCOSMS AND ENRICHMENT CULTURES (B) WHOLECOMMUNITY TRANSCRIPTOMICS AND (C) WHOLE-COMMUNITY PROTEOMICS. ULTIMATELY THE COMBINATION OF BOTH TARGETED AND UNTARGETED APPROACHES WILL PROVIDE ROBUST EVIDENCE OF THE ECOLOGICAL ROLES OF SEVERAL YET-UNCULTIVATED MICROBIAL PHYLA IN GBS AND BEYOND., Reconstructing the universal tree and network of life, G7205239661, G805243471, G834277795, G969889393
OpenAlex ID: W3176018425