Pre-Eukaryotic Cells of the Asgard Superphylum Cultured in Japan!

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BillTre

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Summary
Very exciting finding: Japanese Scientists have cultured cells that are: related to Lokiarchaeota (by genome sequence similarity), have long cellular processes, associate with a bacterium (as a proto-mitochondrion might have.
The origin of advanced eukaryotic cells (that make up all higher organisms (protists, plants, fungi, animals)) have been hypothesized to involve an archaeal cell internalizing a formerly free living alphaproteobacterium. PF threads on this are here and here.

Japanese researchers have isolated archaeal cells, by using culture methods, that are related to Loki--- and have some properties often thought to be found in the pre-eukaryotic host cell. These features include: independently controllable membrane and cytoplasmic regions (protrusions and blebs vs. cell body), mutually beneficial nutrient exchanges with a bacterium.
Science news article here.

Screen Shot 2019-08-10 at 2.37.02 PM.png
Japanese researchers, after working for 12 years, have isolated these difficult to find microbes using a series of cleaver culturing methods. They used anaerobic conditions, methane food source, antibiotics to inhibit bacteria (vs. archaea) and extremely long culture times (since the cells divided about once every two weeks). After setting up several different culture test conditions, they left the cells to grow for about a year and found a single culture with growing cells.

A preprint is available here. In it, the authors, informed by their results, hypothesize how mitochondrial endosymbosis might have occurred:
Screen Shot 2019-08-10 at 3.41.09 PM.png

I'll have to read more of this before I can make any further comments.
 

BillTre

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After reading the preprint in more detail, here are some interesting details from it:

The Prometheoarchaeum syntrophicum cells of this study are not large (less than a micron) and have no internal organelle-like structures, but they do have long branching protrusions. This is interesting because the pre-host cell of the eukaryotic precursors was hypothesized to already have internal membranes (and possibly phagocytosis) since these was thought to enablers of internalizing the pre-mitochondria.
However, having the protrusions, blebs and membrane vaculoes indicates that the pre-host cell probably has a way to make distinct areas of membrane and cytoplasm which could be later elaborated upon duiring the further elaboration of the endosymbiotic relationship. These cytological features could explain why genes indicative of membrane trafficking, vesicle formation/transportation, and cytoskeleton formation were found in the related Lokiarchaeota genome.
The internalization of the eventual future-mitochondrion is instead envisioned as occurring by the protrusions enveloping the pre-mitochondrion rather than the Pre-mitochondrion being engulfed as if it were being eaten. The extra membranes layers resulting from this are hypothesized to form some of the future eukaryotic internal membrane systems.
Although a phagocytosis-like process has been previously proposed6, (i) the observed MK-D1 cells are much too small to engulf their metabolic partner in this way, (ii) Asgard archaea lack phagocytotic machinery, and (iii) a pre-mitochondriate organism lacks sufficient energy to perform phagocytosis. Based on the observation of unusual morphological structures of MK-D1 cells (Fig. 3 and Extended Data Fig. 2), the pre-LECA Asgard archaeon may have produced protrusions and/or MVs (Fig. 5b). For an archaeon syntrophically growing in a narrow space (e.g., sediment pore), it may have been possible for the protrusions/MVs to fuse and inadvertently surround its partner, resulting in phagocytosis-independent engulfment (Fig. 5c)... Such a process would assimilate the partner and simultaneously form a chromosome-bounding membrane structure topologically similar to that of the eukaryotic nuclear membrane (Fig. 5d), a scheme similar to the “Inside-out model” presented by Baum and Baum (2014).
The cells were often (in culture) associated with either sulfur reducing bacteria (Halodesulfovibrio) or a methogenic bacteria (Methanogenium) which could be replaced in culture with a different methanogenic bacteria (Methanobacterium).

They hypothesize the circumstances under which endosymbiosis might have occurred as follows:
  • The ancestral Asgard archaeon was a syntrophic (traded nutrients with another organism) organotroph (obtains hydrogen or electrons from organic compounds for it electron transport respiration).
  • In Earth’s early ocean (no O2), partners were likely methanogenic archaea.
  • As the ocean and atmosphere rose (due to the great oxygenation event), marine sulfate concentrations rose and syntrophy for the Prometheoarchaeum syntrophicum (cells of this study, not the eukaryotic precursor) and likely shifted to interaction with sulfur reducing bacteria.
  • The ancient anaerobic Asgard archaea could have taken one of two paths for survival and adaptation: to remain confined in strictly anaerobic habitats or to advance towards the anoxic-oxic interface with greater substrate and “energy” availability.
  • Prior to endosymbiosis, the pre-LECA archaeon likely interacted with SRB and O2-utilizing organotrophs, who maintained the local habitats O2 concentrations low (Fig. 5b). The O2-utilizing partner was likely a facultative aerobe capable of aerobic and anaerobic H2-generating organotrophy.
  • One of the facultatively aerobic partners was likely the pre-mitochondrial alphaproteobacterium (PA; i.e., future mitochondrion) as it has been proposed that PA would be capable of aerobic and anaerobic H2-generating organotrophy. Evolution of the symbiosis likely led to PA endosymbiosis into the pre-LECA archaeon, resulting in a transitional PA-containing pre-LECA archaeon (PAPLA) using PA as an O2-scavenging and building-block-providing symbiont essential for growth under microaerobic conditions even without SRB.
  • To mature the endosymbiosis, streamlining of metabolic processes is paramount. Two major redundancies are lipid biosynthesis and 2-oxoacid-driven ATP generation. As the hosting PAPLA had ether-type lipids (as evidenced by MK-D1; Fig. 3j) and PA likely had ester-type, two lipid types coexisted in the hybrid cell (Fig. 5d). As horizontal gene transfer between the host and symbiont (or potentially other bacterial source) proceeded, PAPLA likely lost synthesis of ether-type lipids and acquired that of ester-type to resolve redundancy (i.e., streamline genome) in lipid biosynthesis, and passively exchanged the ether-type lipids with ester-type through dilution via cell division (lipid types can mix without compromising structure/fluidity).
This might be taken to imply that the impetus for the formation of endosymbiosuis may have been the great oxygenation event rather than just waiting for the right random events to happen to generate endosymbionts. Taking advantage of (or dealing with) the new oxygenated environments may have driven the initial endosymbiosis.
 
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Ygggdrasil

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The discovery is quite exciting indeed and reflects a huge amount of very careful work. The study provides nice insights into the metabolism and morphology of an Asgard archaeon. I also found their model for eukaryogenesis compelling, especially the thought that during the great oxygenation event, the common ancestor between eukaryotes and the Asgard archaea probably faced a choice between specializing to fill aerobic nices (the path followed by eukaryotes) or anaerobic niches (the path followed by the modern Asgard archaea). Unfortunately, this probably means that the modern, extant Asgard archaea do not completely reflect the ancestral archaea from which eukaryotes evolved. More insight into those ancestral archaea could be inferred by gathering more DNA sequences from other Asgard archaea and combining that genomic information with genomic information from all extant eukaryotes.

One question lacking in the paper is characterizing the function of some of the eukaryote-specific genes found in the MK-D1 cells. Of course, those experiments would likely necessitate genetic manipulations, which would be very difficult to perform given the ~month long doubling times.

Regarding internal membranes in prokaryotes, another preprint was published recently reporting the discovery of a bacterium containing an internal membrane enclosing its nucleoid.

Katayama et al. Membrane-bounded nucleoid discovered in a cultivated bacterium of the candidate phylum ‘Atribacteria’. bioRxiv 2019. https://www.biorxiv.org/content/10.1101/728279v1.full

Abstract:
A key feature that differentiates prokaryotes from eukaryotes is the absence of an intracellular membrane surrounding the chromosomal DNA. Here, we report isolation of an anaerobic bacterium that possesses an additional intracytoplasmic membrane surrounding a nucleoid, affiliates with the yet-to-be-cultivated ubiquitous phylum ‘Ca. Atribacteria’, and possesses unique genomic features likely associated with organization of complex cellular structure. Exploration of the uncharted microorganism overturned the prevailing dogma of prokaryotic cell structure.
These bacteria likely were not involved in eukaryogenesis as they seem to belong to a separate branch than the alphaproteobacteria that eventually fused with the Asgard archaea to become mitochondria. However, it does suggest that nucleus-like structures and other internal membrane systems could exist in other bacteria and archaea, providing potential explanations for the evolution of the nucleus and internal membrane systems of eukaryotes. It would be interesting to discover the genes involved in the formation of the nucleus in these Atribacteria and determine whether they exist in other prokaryotic species.
 

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