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Monday 24 March 2014

And Fuerst strikes back

Planctomycetes are definitively fascinating bacteria. In addition to other interesting characteristics, the exact definition of their cell plan appears to continues to baffle biologists. Initially, back at the end of last century and beginning of this one, Planctomycetes have been claimed to possess a particular cell plan, differentiating them from classical bacterial ones, mainly based on the work of Fuerst and colleagues.
Last year and beginning of this one (2013-14), Devos and associates have published a series of paper advocating that the cell plan of those bacteria is not so radically different, but a variation from, the classical Gram-negative cell plan (see previous posts on the subject here and there). This claim has been developed in various articles and was based on reconsideration of the previous data from Fuerst and others, taking into account novel data, including genomics and high resolution electron-microscopy. This claim had been voiced by others before (Speth et al., Front. Microbiol. 2012; Strous et al., Nature 2006; Lage et al AvL 2013), causing considerable trouble in the PVC community.
Now Fuerst just struck back with new electron-microscopy and immuno-localization data combined with a new model of division in Gemmata obscuriglobus, just published in Sagulenko et al., PLoS One 2014.
The data is highly interesting, including that in some of the supplementary movies, you can see the tubulovesicular network previously revealed by Acehan et al. (particularly in SMovie 2). However, they appear far from being conclusive and promise to fuel more controversy instead of settling it.
In addition, to the interesting data about the cell plan, the cell wall (Suppl. fig. 4), and the FtsK data, Fuerst present a re-evaluated model of cell division in Gemmata (see figure)
The presented three-dimensional reconstruction of a 'nuclear body' does indeed appear to confirm, at least in the presented case, the presence of such compartment in this organism, although more details about the metodology and data would have been needed to fully appreciate the accuracy and relevance of the model. However the data could also be interpreted in the tubulo-vesicular model of Acehan et al., were the DNA containing compartment would just be another of the connected vesicles that fill the cytoplasm, a derivation of the G- cell cycle, as proposed by Devos TiM 2014 (see figure).

Figure 4: A model for mechanism of cell division of G. obscuriglobus cells.
Step 1, the bud appears as a hump on the surface of a cell (Figures S5 and S6 in File S1). The nuclear body is divided, before or during the formation of a bud, forming two fully enveloped structures, as shown in step 2. Finally, one of the nuclear bodies migrates into a newly formed cell (step 3). Other riboplasm vesicles not containing nucleoid DNA are also transferred into the newly formed cell (Figure S6B in File S1). Cell wall is indicated in red; plasma membrane – blue; ICM – green; paryphoplasm – yellow; riboplasm – light blue; nucleoid – black; ribosomes – grey circles. doi:10.1371/journal.pone.0091344.g004.
This is the legend directly from the article. In the G- interpretation, Riboplasm=Cytoplasm; Paryphoplasm=Periplasm.
Despite the wealth of interesting data, some contradictions are found in the paper and it gives the impression to have been written in a haste, throwing together data that could have made it to a few independent paper if consolidated by more results. May be the most important contradiction is the comparison between the topology of the 'nuclear body' and the one of the eukaryotic nucleus, a subject very dear to Fuerst.
The authors constantly claim that the 'nuclear body' is mostly separated from the rest of the cytoplasm by a double membrane, including nice figures seemingly confirming this. However, it seems that this double membrane is in fact formed by the juxtaposition of the membranes of two vesicles or compartments, as acknowledged by the authors (see figure).
If we stick to this interpretation, then the 'nuclear-body' is mostly surrounded by a single-membrane, and not a double one. And as such, there is limited similarity with the eukaryotic nuclear envelope and the nucleus.
This has also implications for the mode of division of this bacteria that has lost the classical FtsZ-based division machinery and the proposed model definitively deserves consideration.
All together, a very interesting paper that deserves to be read very carefully. Even if it seems like a melting-pot of various subjects, the presented data are of considerable interest. However, it clearly does not settle the issue about PVC cell plan or its mode of division. The proposed models are at best tentative and more work is definitively required on both subjects.

I would very much like to encourage you to post a comment about your reaction to this paper and may be to start a discussion about it.