Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction

Abstract

Marine and estuary sediments contain a variety of uncultured archaea whose metabolic and ecological roles are unknown. De novo assembly and binning of high-throughput metagenomic sequences from the sulfate-methane transition zone in estuary sediments resulted in the reconstruction of three partial to near-complete (2.4-3.9 Mb) genomes belonging to a previously unrecognized archaeal group. Phylogenetic analyses of ribosomal RNA genes and ribosomal proteins revealed that this group is distinct from any previously characterized archaea. For this group, found in the White Oak River estuary, and previously registered in sedimentary samples, we propose the name 'Thorarchaeota'. The Thorarchaeota appear to be capable of acetate production from the degradation of proteins. Interestingly, they also have elemental sulfur and thiosulfate reduction genes suggesting they have an important role in intermediate sulfur cycling. The reconstruction of these genomes from a deeply branched, widespread group expands our understanding of sediment biogeochemistry and the evolutionary history of Archaea.

Figure 1

Phylogenetic position of the full-length 16S rRNA gene from the SMTZ1-83 genomic bin within the Archaea. The other two bins contain 16S rRNA gene <900 bp, thus were not included in this analysis. Bin SMTZ1-45 contains 682 bp of a 16S rRNA gene. The tree was generated using RAxML in the ARB software package (Ludwig et al., 2004). Closed and open circles represent bootstraps >80% and >60% (respectively) generated using IQtree (Nguyen et al., 2015). Closed circles represent bootstrap values of >70%. Giardia lamblia was used as the outgroup.

Figure 2

Phylogenetic analysis of 16 concatenated ribosomal proteins (rpL2, 3, 4, 5, 6, 14, 15, 16, 18, 22, 24 and rpS3, 8, 10, 17, 19) generated using RAxML in the ARB software package. Closed and open circles represent bootstraps >80% and >60% (respectively) generated using IQtree (Nguyen et al., 2015).

Figure 3

Domain-level taxonomic distribution of top hits to genes in the three Thorarchaeota genomes, based on nucleotide comparisons (BLASTn) of the genes with those present in Genbank (NCBI, nt database).

Figure 4

Metabolic reconstruction of the Thorarchaeaota genomic bin (SMTZ1-83) based on genes identified using the KEGG database. Genes for various metabolisms, importers and hydrogenases are represented. White boxes represent the genes that are present in the genome and gray boxes represent genes that are absent. Details about the genes numbered are provided in Supplementary Table S2.