Category Archives: Archaeans

We all came from Asgard

by Piter Kehoma Boll

And by “we all” I mean we, the eukaryotes, the organisms with complex cells with a nucleus, mitochondria and stuff.

The way organisms are classified changed hugely across the last two centuries but, during the past few decades, it became clear that we have three domains of life, namely Bacteria, Archaea and Eukarya. Although the relationship between these three domains was problematic at first, it soon became clear that Eukarya and Archaea are more closely related to each other than they are to Bacteria.

Both Bacteria and Archaea are characterized by the so-called prokaryotic cell, in which there is no delimited nucleus and only a single circular chromosome (plus a lot of smaller gene rings called plasmids). Eukarya, on the other hand, has a nucleus surrounded by a membrane which includes many linear chromosomes. Both the structure of the cell membrane and several genes indicate that Archaea and Eukarya are closely related, but it was still a mystery whether both groups evolved from a common ancestor and were, therefore, sister-groups, or whether eukaryotes evolved directly from archaeans and were, therefore, highy complex archaeans.

Things started to point toward the second hypothesis after several proteins originally considered exclusive to eukaryotes (the so-called Eukaryotic Signature Proteins, ESPs) were found in representatives of the clade TACK of Archaea. However, different clades within the TACK clade had different ESPs, so things remained uncertain.

Then in 2015 a new group of archaeans was discovered in the Arctic Ocean between Norway an Greenland near a field of active hydrothermal vents named Loki’s Castle (Spang et al. 2015). Named Lokiarchaeoata, this new archaean group contained a larger number of ESPs, including many found in different TACK lineages. Lokiarchaeota appeared as a sister-group of eukaryotes in phylogenetic reconstructions and indicated that eukaryotes evolved, indeed, from archaeans, and apparently from more complex archaeans than the ones known at the time. This group was solely based on an incomplete genome found in the sediments, as the organism itself was not found and could not be cultivated to confirm the structure of its cell.

In 2016, another new archaean lineage was discovered through a genome found in the White Oak River estuary on the Atlantic coast of the USA (Seitz et al., 2016). Named Thorarchaeota, this clade revealed to be closely related to Lokiarchaeota and, therefore, to Eukaryotes.

Reconstruction of possible metabolic routes found in Thorarchaeota based on the genes (white boxes) found in the thorarchaeotan genome. Credits to Seitz et al. (2016).

Then in 2017 a lot of new genomes were found in the same environments in which Lokiarchaeaota and Thorarchaeota had been found and in many others (Zaremba-Niedzwiedzka et al., 2017). They included two new groups closely related to these two, which were named Odinarchaeota and Heimdallarchaeota. This whole group received the name “Asgard archaeans” and phylogenetic reconstructions put Eukarya within it, with Heimdallarchaeota being Eukarya’s sister group.

But questions and doubts soon arised. Still in 2017, a new paper (Da Cunha et al., 2017) questioned these findings and raised the hypothesis that the phylogenetic reconstructions putting Asgard and Eukarya together was an artifact caused by long branch attraction, a side-effect of phylogenetic reconstructions in which fast-evolving species force distantly related clades to collapse into a single clade. The removal of some fast-evolving archaeans from the analysis was enough to break the Asgard-Eukarya relationship apart. Since the genomes of Lokiarchaeota and other Asgards were reconstructed from environmental DNA and not from single cells, there was a possibility that the samples were contaminated with material from other organisms. The protein genes used in the analyses also seemed to have divergent origins and may have been acquired via horizontal gene transfer, when a gene is transferred from one organism to another by means other than reproduction, usually through viruses.

The original authors of the Asgard clade, who proposed its proximity to Eukarya, rejected Da Cunha et al.’s (2017) criticism and stated that they used inadequate methodology and that there was no evidence of contamination in their samples (Spang et al., 2018).

(OMG, this turned into an actual fight. Grab your popcorns!)

Da Cunha et al. (2018) responded again showing more evidence of contamination and saying that Spang et al. should show evidence of inadequate methodology if it was the case.

Later studies continued to find the eukaryote sequences in new samples of Asgard, which decrease the likelihood of contamination (Narrowe et al., 2018).

Fournier & Poole (2018) discussed the implications of the proximity of Eukarya to Asgard and proposed a classification in which Asgard was not a member of Archaea anymore, but formed a new domain, Eukaryomorpha, together with Eukarya. They made an analogy with the mammals evolving from synapsids and how synapsids used to be seen as reptiles, even though they are not nested inside the Reptilia (Sauropsida) clade. The same would be the case of Asgard. Despite being “Archaea-like”, they would not be true archaeans.

A hypothetical topology of “true archaeans”, Asgard and Eukarya according to Fournier & Poole (2018).

In a study published in December, Williams et al. (2019) reanalyzed the issue using more data and recovered again the proximity of Asgard to Eukarya. With this accumulation of evidence, the hypothesis of Eukarya originating from inside Archaea grew stronger.

Then now, a few days ago, we finally got what we were waiting for. A group of Japanese scientists (Imachi et al., 2020) finally isolated an Asgard organism and was able to culture it in the lab. It was a very hard task, though. The culture grew very slowly, with a lag phase (the phase in which cells adapt to the environment and grow without dividing) lasting up to 60 days!

The creatures were growing in a mixed culture with a bacterium of the genus Halodesulfovibrio and an archaeon of the genus Methanogenium. The Asgard cells were named Candidatus Prometheoarcheum syntrophicum. In prokaryote taxonomy, a new species receives the status of Candidatus when it was not possible to maintain it in a stable culture.

The cells of this Asgard species are coccoid, i.e., spherical, and often present vesicles on the surface or long membrane protrusions that may or not branch. These protrustions do not connect to each other nor to other cells, differently from similar structures in other archaeans. The cells do not seem to contain any organelle-like structures inside them, going against the expectations. Asgard is not yet the eukaryote-like cell we were waiting for!

Several electron microscope images of Canidatus Prometheoarcheum syntrophicum. Vesicles show in e, f and proturision in g, h. Credits to Imachi et al. (2020).

Thanks to the culture of this Asgard species, it was possible to extract its whole genome and confirm what was previously known from Asgard and based solely on environmental DNA. This confirmed the presence of 80 ESPs and, in a phylogenetic analysis, this new species appeared as the sister group of Eukarya.

Candidatus Prometheoarcheum syntrophicum revealed to be anaerobic and to feed on aminoacids, breaking them into fatty acids and hydrogen. Its association with the other two prokariotes in the mixed culture seems to be a sort of mutualism, with the three species helping each other by hydrogen transfer from one species to another. Many questions about how an organism like that turned into the complex eukaryotic cell still remain but at least we have some more hints about the acquisition of the mitochondria.

Hypothesis of eukaryotic cell evolution based on a mutualistic relationship between an Asgard-like archaean and an aerobic bacterium. Credits to Imachi et al. (2020).

The most widely accepted hypothesis was that primitive eukaryotic cells engulfed an aerobic bacteria through phagocytosis to eat it but ended up retaining it inside. However, seeing the cooperation of our Asgard archaean with other prokaryotes raises the hypothesis that maybe the mutualism between the pro-eukaryotic cell and the aerobic bacteria started when they were still separate organisms.

Are we ever going to find the “true” proto-eukaryote? Let’s wait for the next episodes.

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References:

Da Cunha V, Gaia M, Gadelle D, Nasir A, Forterre P (2017) Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLOS Genetics 13(6): e1006810. doi: 10.1371/journal.pgen.1006810

Da Cunha V, Gaia M, Nasir A, Forterre P (2018) Asgard archaea do not close the debate about the universal tree of life topology. PLOS Genetics 14(3): e1007215. doi: 10.1371/journal.pgen.1007215

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

Narrowe AB, Spang A, Stairs CW, Caceres EF, Baker BJ, Miller SC, Ettema TJG (2018) Complex Evolutionary History of Translation Elongation Factor 2 and Diphthamide Biosynthesis in Archaea and Parabasalids. Genome Biology and Evolution 10: 2380–2393. doi: 10.1093/gbe/evy154

Seitz KW, Lazar CS, Hinrichs KU, Teske AP, Baker BJ (2016) Genomic reconstruction of a novel, deeply branched sediment archaeal plylum with pathways for acetogenesis and sulfur reduction. ISME Journal 10: 1696–1705. doi: 10.1038/ismej.2015.233

Spang A, Saw JH, Jørgensen SL, et al. (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521: 173–179. doi: 10.1038/nature14447

Spang A, Eme L, Saw JH, Caceres EF, Zaremba-Niedzwiedzka K, et al. (2018) Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLOS Genetics 14(3): e1007080. doi: 10.1371/journal.pgen.1007080

Williams TA, Cox CJ, Foster PG, Szőllősi GJ, Embley TM (2019) Phylogenomics provides robust support for a two-domains tree of life. Nature Ecology & Evolution. doi: 10.1038/s41559-019-1040-x

Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al. (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358. doi: 10.1038/nature21031

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Friday Fellow: Walsby’s Square Haloarchaeon

by Piter Kehoma Boll

After more than a hundred Friday Fellows, there is still one group with no representatives here: the archaeans. But this is going to change today with the indroduction of our first Friday Fellow archaean, and it is a very interesting one for sure.

Scientifically known as Haloquadratum walsbyi, it is sometimes called Walsby’s Square Haloarchaeon and, as its name suggest, it has an unusual square shape.

haloquadratum_walsbyi00

A drawing showing a set of four cells of Walby’s square haloarchaeon.

This interesting archaean was discovered in 1980 by Anthony Edward Walsby in brine ponds of the Sinai Peninsula. It was later discovered in several other lakes with high concentrations of salt around the world and was first cultivated in the laboratory in 2004, but only in 2007 it was formally described and received a binomial name.

The square cells of the Walsby’s square haloarchaeon are very thin, about 0.2 µm thick, and measure about 2 µm on each side. They grow very slowly, forming a thin sheet over a surface, the largest recorded sheet measuring 40 × 40 µm. If the growing conditions are not ideal, the cells deteriorate to a ragged square or other shapeless flat form.

Haloquadratum

Photographs of cells of Haloquadrum walsbyi showing the crystal-shaped air vacuoles. Image extracted from Burns et al. (2007).

Inside the cells, the Walsby’s square haloarchaeon has small gas vesicles that look like small crystals. They help the cell remain at the surface of the very salty water they inhabit. In order to survive, this archaean needs water with a concentration of salt of at least 14%, but the conditions become ideal only above 23%.

Although we know some interesting things about this species, there is still much more to learn. Who knows what mysteries this small square-shaped creature is hiding from us?

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References:

Bolhuis, H.; Poele, E. M. t.; Rodriguez-Valera, F. (2004) Isolation and cultivation of Walsby’s square archaeonEnvironmental Microbiology 6(12): 1287–1291.

Burns, D. G.; Janssen, P. H.; Itoh, T.; Kamekura, M.; Li, Z.; Jensen, G.; Rodríguez-Valera, F.; Bolhuis, H.; Dyall-Smith, M. L. (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and SpainInternational Journal of Systematic and Evolutionary Microbiology 57: 387–392.

 

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Filed under Archaeans, Friday Fellow