Candidatus Prometheoarchaeum

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Classification

A scanning electron microscopy image of Prometheoarchaeum syntrophicum. (Hiroyuki Imachi, Masaru K. Nobu and JAMSTEC 2020)

Domain: Archaea

Kingdom: Proteoarchaeota

Superphylum: Asgard

Phylum: Lokiarchaeota

Genus: Candidatus

Species: Prometheoarchaeum syntrophicum "Imachi et al. 2020"

Strain: MK-D1

Use NCBI link to find]

Species

NCBI: Taxonomy

Candidatus Prometheoarchaeum syntrophicum strain MK-D1

Description and Significance

Describe the appearance, habitat, etc. of the organism, and why you think it is important.

From deep-sea sediments to a bioreactor-based “pre-enrichment” and a final seven-year in vitro enrichment Hiroyuki Imachi dubbed the newly cultured and isolated Lokiarchaeon, “Candidatus Prometheoarchaeum syntrophicum strain MK-D1”. Current data suggest that this archaeal lineage known as "Asgard archaea" may have given rise to eukaryotes (Spang A. et al. 2015). Although a resemblance of eukaryote-like genomic features have been discovered in these archaea, the evolutionary transition from archaea to eukaryotes remains uncertain due to the lack of cultured representatives and corresponding physiological insights. Given the proposed eukaryote-like intracellular complexities for Asgard archaea, the MK-D1 isolate has no visible organelle-like structure. Morphological features of Candidatus Prometheoarchaeum syntrophicum are of unique complexity; long and branching protrusions.

Genome Structure

Phylogeny of MK-D1 and catabolic features of Asgard archaea.

Genomes for Ca. Prometheoarchaeum syntrophicum MK-D1, Halodesulfovibrio sp. MK-HDV, and Methanogenium sp. MK-MG are available under Genbank BioProjects PRJNA557562, PRJNA557563, and PRJNA557565 respectively. The iTAG sequence data was deposited in Bioproject PRJDB8518 https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJDB8518 with the accession numbers DRR184081–DRR184101. The 16S rRNA gene sequences of MK-D1, Halodesulfovibrio sp. MK-HDV, Methanogenium sp. MK-MG and clones obtained from primary enrichment culture were deposited in the DDBJ/EMBL/GenBank database http://getentry.ddbj.nig.ac.jp under accession numbers LC490619–LC490624.


The MK-D1 cell envelope may be composed of a membrane and a surrounding S-layer, given the presence of four genes that encode putative S-layer proteins, stalk-like structures on the surface of the vesicles, and the even distance between the inner and outer layers of the cell envelope.



The evolutionary relationship between archaea and eukaryotes has been under debate, hinging on the incompleteness and contamination associated with metagenome-derived genomes and variation in results depending on tree construction protocols20–23. By isolating strain MK-D1, we were able to obtain a closed genome (Supplementary Table S1 and Fig. S1) and construct a ribosomal protein-based phylogenomic tree that shows clear phylogenetic sistering between MK-D1 and Eukarya (Fig. 4a and Supplementary Tables S4 and S5, and Fig. S4). Thus, strain MK-D1 represents the closest cultured archaeal relative of eukaryotes. We confirmed the presence of many ESPs identified in related Asgard archaea (Supplementary Fig. S5) and obtained the first RNA-based evidence for expression of such genes (Supplementary Table S6).

Cell Structure, Metabolism and Life Cycle

Syntrophic amino acid utilization of MK-D1.
Microscopic characterization and lipid composition of MK-D1.

Candidatus Prometheoarchaeum syntrophicum’ strain MK-D1 is an anaerobic, extremely slow-growing, small coccus (around 550 nm in diameter) that degrades amino acids through syntrophy. Microscopic observations suggest that the cells are small cocci, ca. 300-750 nm in diameter (average 550 nm, n=15), and generally form aggregates surrounded with extracellular polysaccharide-like materials. The cells also form unique membrane-based protrusions with a diameter of about 80–100 nm and various lengths (Aoki, M. et al 2014). The morphological compositions of MK-D1 is unique in comparison to known archaeal protrusions (Marguet, E. et al 2013.) Dividing cells have less EPS-like materials and a ring-like structure around the middle of cells.

Cryo-electron and transmission electron microscopic observations revealed that the cells contain no visible organelle-like inclusions (Fig. 3d–f, Extended Data Fig. 2. The cells produce membrane vesicles (MVs; 50–280 nm in diameter) (Fig. 3d–f and Extended Data Fig. 2) and chains of blebs (Fig. 3c and Extended Data Fig. 2e). The cells unique membrane-based protrusions with a diameter of about 80–100 nm and various lengths are illustrated. (Fig. 3g–i and Extended Data Fig. 2). Some protrusions remarkably display complex branching, unlike known archaeal protrusions. These protrusions are especially abundant after late exponential growth phase. Lipid composition analysis of the MK-D1 and Methanogenium co-culture revealed typical archaeal signatures – a C20-phytane and C40-biphytanes (BPs) with 0–2 cyclopentane rings (Fig. 3j). Considering the lipid data obtained from a reference Methanogenium isolate (99.3% 16S rRNA gene identity; Supplementary Fig. S3), MK-D1 probably contains C20-phytane and C40-BPs with 0–2 rings.

Ecology and Pathogenesis

Habitat; symbiosis; biogeochemical significance; contributions to environment.
If relevant, how does this organism cause disease? Human, animal, plant hosts? Virulence factors, as well as patient symptoms.

MK-D1 was isolated from deep-sea methane seep sediment of the Nankai Trough at 2533 m water depth, off Kumano area, Japan.

Based on cultivation and genomics, we propose an “Entangle-Engulf-Enslave (E3) model” for eukaryogenesis through archaea-alphaproteobacteria symbiosis mediated by the physical complexities and metabolic dependency of the hosting archaeon.

References

Imachi H, Nobu MK, Nakahara N, et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature. 2020;577(7791):519‐525. doi:10.1038/s41586-019-1916-6

Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).

Aoki, M. et al. A long-term cultivation of an anaerobic methane-oxidizing microbial community from deep-sea methane-seep sediment using a continuous-flow bioreactor. PLoS ONE 9, e105356 (2014).

Marguet, E. et al. Membrane vesicles, nanopods and/or nanotubes produced by hyperthermophilic archaea of the genus Thermococcus. Biochem. Soc. Trans. 41, 436–442 (2013).



Author

Page authored by Jeremy Eugene Patrick, student of Prof. Jay Lennon at Indiana University.