Lokiarchaeota

Lokiarchaeota is a proposed phylum of the Archaea.[1] The phylum includes all members of the group previously named Deep Sea Archaeal Group (DSAG), also known as Marine Benthic Group B (MBG-B). A phylogenetic analysis disclosed a monophyletic grouping of the Lokiarchaeota with the eukaryotes. The analysis revealed several genes with cell membrane-related functions. The presence of such genes support the hypothesis of an archaeal host for the emergence of the eukaryotes; the eocyte-like scenarios.

Lokiarchaeota
Scientific classification
Domain:
Archaea
Kingdom:
"Proteoarchaeota"
Superphylum:
Asgard
Phylum:
"Lokiarchaeota"

Spang et al. 2015
Type species
Candidatus Prometheoarchaeum syntrophicum
Genus
  • "Candidatus Lokiarchaeum" Spang et al. 2015
  • "Candidatus Prometheoarchaeum" Imachi et al. 2020

Lokiarchaeota was introduced in 2015 after the identification of a candidate genome in a metagenomic analysis of a mid-oceanic sediment sample. This analysis suggests the existence of a genus of unicellular life dubbed Lokiarchaeum. The sample was taken near a hydrothermal vent at a vent field known as Loki's Castle located at the bend between Mohns/Knipovitch ridge in the Arctic Ocean.[2]

Discovery

Sediments from a gravity core taken in 2010 in the rift valley on the Knipovich ridge in the Arctic Ocean, near the so-called Loki's Castle hydrothermal vent site, were analysed. Specific sediment horizons, previously shown to contain high abundances of novel archaeal lineages[3][4] were subjected to metagenomic analysis. Due to the low density of cells in the sediment, the resulting genetic sequence does not come from an isolated cell, as would be the case in conventional analysis, but is rather a combination of genetic fragments.[5] The result was a 92% complete, 1.4 fold-redundant composite genome named Lokiarchaeum.[2]

The metagenomic analysis determined the presence of an organism's genome in the sample.[2] However, the organism itself was not cultured until years later, with a Japanese group first reporting isolation and cultivation of a Lokiarcheota strain in 2019.[6]

The Lokiarchaeota phylum was proposed based on phylogenetic analyses using a set of highly conserved protein-coding genes.[2] Through a reference to the hydrothermal vent complex from which the first genome sample originated, the name refers to Loki, the Norse shape-shifting god.[5] The Loki of literature has been described as "a staggeringly complex, confusing, and ambivalent figure who has been the catalyst of countless unresolved scholarly controversies",[7] an analogy to the role of Lokiarchaeota in debates about the origin of eukaryotes.[2]

Description

The Lokiarchaeum composite genome consists of 5,381 protein coding genes. Of these, roughly 32% do not correspond to any known protein, 26% closely resemble archaeal proteins, and 29% correspond to bacterial proteins. This situation is consistent with: (i) proteins from a novel phylum (with few close relatives, or none) being difficult to assign to their correct domain; and (ii) existing research that suggests there has been significant inter-domain gene transfer between bacteria and Archaea.

A small, but significant portion of the proteins (175, 3.3%) that the recovered genes code for are very similar to eukaryotic proteins. Sample contamination is an unlikely explanation for the unusual proteins because the recovered genes were always flanked by prokaryotic genes and no genes of known eukaryotic origin were detected in the metagenome from which the composite genome was extracted. Further, previous phylogenetic analysis suggested the genes in question had their origin at the base of the eukaryotic clades.[2]

In eukaryotes, the function of these shared proteins include cell membrane deformation, cell shape formation, and a dynamic protein cytoskeleton.[2][8][9] It is inferred then that Lokiarchaeum may have some of these abilities.[2] Another shared protein, actin, is essential for phagocytosis in eukaryotes.[5][8] Phagocytosis is the ability to engulf and consume another particle; such ability would facilitate the endosymbiotic origin of mitochondria and chloroplasts, which is a key difference between prokaryotes and eukaryotes.[2]

Evolutionary significance
A schematic evolutionary tree of the archaea including Lokiarchaeota and the root of eukaryotes[2]

A comparative analysis of the Lokiarchaeum genome against known genomes resulted in a phylogenetic tree that showed a monophyletic group composed of the Lokiarchaeota and the eukaryotes,[10] supporting an archaeal host or eocyte-like scenarios for the emergence of the eukaryotes.[11][12][13] The repertoire of membrane-related functions of Lokiarchaeum suggests that the common ancestor to the eukaryotes might be an intermediate step between the prokaryotic cells, devoid of subcellular structures, and the eukaryotic cells, which harbor many organelles.[2]

Carl Woese's three-domain system classifies cellular life into three domains: archaea, bacteria, and eukaryotes; the last being characterised by large, highly evolved cells, containing mitochondria, which help the cells produce ATP (adenosine triphosphate, the energy currency of the cell), and a membrane-bound nucleus containing nucleic acids. Protozoa and all multicellular organisms such as animals, fungi, and plants are eukaryotes.

The bacteria and archaea are thought to be the most ancient of lineages,[14] as fossil strata bearing the chemical signature of archaeal lipids have been dated back to 3.8 billion years ago.[15] The eukaryotes include all complex cells and almost all multicellular organisms. They are considered to have evolved between 1.6 and 2.1 billion years ago.[16] While the evolution of eukaryotes is considered to be an event of great evolutionary significance, no intermediate forms or "missing links" had been discovered previously. In this context, the discovery of Lokiarchaeum, with some but not all of the characteristics of eukaryotes, provides evidence on the transition from archaea to eukaryotes.[17] Lokiarchaeota and the eukaryotes probably share a common ancestor, and if so, diverged roughly two billion years ago. This putative ancestor possessed crucial "starter" genes that enabled increased cellular complexity. This common ancestor, or a relative, eventually led to the evolution of eukaryotes.[5]

In 2019, a Japanese research group reported culturing a strain of Lokiarcheota in the laboratory. This strain, currently named Candidatus Prometheoarchaeum syntrophicum strain MK-D1, was observed in syntrophic association with two hydrogen-consuming microbes: a sulfate-reducing bacteria of the genus Halodesulfovibrio and a methanogen of the genus Methanogenium. The MK-D1 organism produces hydrogen as a metabolic byproduct, which is then consumed by the symbiotic syntrophs. MK-D1 also seems to organize its external membrane into complex structures using genes shared with eukaryotes. While association with alphaproteobacteria (from which mitochondria are thought to descend) was not observed, these features suggest that MK-D1 and its syntrophs may represent an extant example of archaea-bacteria symbiosis similar to that which gave rise to eukaryotes. The research behind this report, after being peer-reviewed, has now been published.[18][19][6]

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References
  1. Lambert, Jonathan (9 August 2019). "Scientists glimpse oddball microbe that could help explain rise of complex life - 'Lokiarchaea', previously known only from DNA, is isolated and grown in culture". Nature. 572: 294. Bibcode:2019Natur.572..294L. doi:10.1038/d41586-019-02430-w. PMID 31409927. Retrieved 10 August 2019.
  2. Spang, Anja; Saw, Jimmy H.; Jørgensen, Steffen L.; Zaremba-Niedzwiedzka, Katarzyna; Martijn, Joran; Lind, Anders E.; van Eijk, Roel; Schleper, Christa; Guy, Lionel; Ettema, Thijs J. G. (2015). "Complex archaea that bridge the gap between prokaryotes and eukaryotes". Nature. 521 (7551): 173–179. Bibcode:2015Natur.521..173S. doi:10.1038/nature14447. ISSN 0028-0836. PMC 4444528. PMID 25945739.
  3. Jørgensen, Steffen Leth; Hannisdal, Bjarte; Lanzen, Anders; Baumberger, Tamara; Flesland, Kristin; Fonseca, Rita; Øvreås, Lise; Steen, Ida H; Thorseth, Ingunn H; Pedersen, Rolf B; Schleper, Christa (September 5, 2012). "Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge". PNAS. 109 (42): E2846–55. doi:10.1073/pnas.1207574109. PMC 3479504. PMID 23027979.
  4. Jørgensen, Steffen Leth; Thorseth, Ingunn H; Pedersen, Rolf B; Baumberger, Tamara; Schleper, Christa (October 4, 2013). "Quantitative and phylogenetic study of the Deep Sea Archaeal Group in sediments of the Arctic mid-ocean spreading ridge". Frontiers in Microbiology. 4: 299. doi:10.3389/fmicb.2013.00299. PMC 3790079. PMID 24109477.
  5. Rincon, Paul (May 6, 2015). "Newly found microbe is close relative of complex life". BBC. Retrieved May 9, 2015.
  6. Imachi, Hiroyuki; et al. (15 January 2020). "Isolation of an archaeon at the prokaryote–eukaryote interface". Nature. 577: 519–525. bioRxiv 10.1101/726976. doi:10.1038/s41586-019-1916-6. PMC 7015854. PMID 31942073. Retrieved 15 January 2020.
  7. von Schnurbein, Stefanie (November 2000). "The Function of Loki in Snorri Sturluson's "Edda"". History of Religions. 40 (2): 109–124. doi:10.1086/463618.
  8. Ghoshdastider U, Jiang S, Popp D, Robinson RC (2015). "In search of the primordial actin filament". Proc Natl Acad Sci U S A. 112 (30): 9150–1. doi:10.1073/pnas.1511568112. PMC 4522752. PMID 26178194.CS1 maint: uses authors parameter (link)
  9. Khan, Amina (May 6, 2015). "Meet Loki, your closest-known prokaryote relative". LA Times. Retrieved May 9, 2015.
  10. Maximillan, Ludwig (27 December 2019). "Evolution: A revelatory relationship". Phys.org. Retrieved 28 December 2019.
  11. Embley, T. Martin; Martin, William (2006). "Eukaryotic evolution, changes and challenges". Nature. 440 (7084): 623–630. Bibcode:2006Natur.440..623E. doi:10.1038/nature04546. ISSN 0028-0836. PMID 16572163.
  12. Lake, James A. (1988). "Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences". Nature. 331 (6152): 184–186. Bibcode:1988Natur.331..184L. doi:10.1038/331184a0. ISSN 0028-0836. PMID 3340165.
  13. Guy, Lionel; Ettema, Thijs J.G. (2011). "The archaeal 'TACK' superphylum and the origin of eukaryotes". Trends in Microbiology. 19 (12): 580–587. doi:10.1016/j.tim.2011.09.002. ISSN 0966-842X. PMID 22018741.
  14. Wang, Minglei; Yafremava, Liudmila S.; Caetano-Anollés, Derek; Mittenthal, Jay E.; Caetano-Anollés, Gustavo (2007). "Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world". Genome Research. 17 (11): 1572–1585. doi:10.1101/gr.6454307. PMC 2045140. PMID 17908824.
  15. Hahn, Jürgen; Haug, Pat (1986). "Traces of Archaebacteria in ancient sediments". Systematic and Applied Microbiology. 7 (Archaebacteria '85 Proceedings): 178–83. doi:10.1016/S0723-2020(86)80002-9.
  16. Knoll, Andrew H.; Javaux, E. J.; Hewitt, D.; Cohen, P. (29 June 2006). "Eukaryotic organisms in Proterozoic oceans". Philosophical Transactions of the Royal Society B. 361 (1470): 1023–38. doi:10.1098/rstb.2006.1843. PMC 1578724. PMID 16754612.
  17. Zimmer, Carl (6 May 2015). "Under the Sea, a Missing Link in the Evolution of Complex Cells". New York Times. Retrieved 8 May 2015.
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