Quick guide to Gemmata obscuriglobus

A beginner's guide to our favorite bacterium has just been released in Current Biology. This is the perfect starting point if you are interested in microbiology's platypus. Current Biology's Quick Guides aim to give readers 'everything you need to know about...' for topics they're likely to see fairly regularly in major journals but aren't up to speed with. This one starts like this "What is Gemmata obscuriglobus? Gemmata obscuriglobus is the standard bearer of a group of bacteria that has recently been the focus of interest in cellular, environmental, medical and evolutionary biology. G. obscuriglobus bacteria have been dubbed the ‘platypus of microbiology’ because of their peculiar characteristics usually not observed in bacteria, including some that are more commonly associated with eukaryotes and archaea."

Three-Dimensional Reconstruction of Bacteria with a Complex Endomembrane System

That is it, our last paper is out, Santarella-Mellwig et al., PLoS Biology 2013. In this paper, we investigated the three-dimensional organization of the complex endomembrane system in the planctomycete bacterium Gemmata obscuriglobus. We reveal that the G. obscuriglobus cells are neither compartmentalized nor nucleated, contrary to previous claims, as none of the spaces created by the membrane invaginations is topologically closed; instead, they are all interconnected. The organization of cellular space is similar to that of a classical Gram-negative bacterium modified by the presence of large invaginations of the inner membrane inside the cytoplasm. Thus, the membrane organization of G. obscuriglobus, and most likely all PVC members, is not fundamentally different from, but is rather an extension of, the “classical” Gram-negative bacterial membrane system.

See also the blog post cleaverly entitled Bacterium excluded from the Eukaryote Club

How do Planctomycetes divide?

One of the particular features of Planctomycetes, and some other PVCs, is that they have lost the otherwise ubiquitous FtsZ gene. FtsZ is the main building block of the constriction ring that all other bacterial cells use to divide by fission. It is so important that it is one of the few proteins that are found in all bacteria, with very few exceptions. One of them, of course, are some of the PVCs, and in particular almost all Planctomycetes. And we know they have lost it, because the dcw cluster is still present but showing different degrees of erosion in actual PVCs, demonstrating that it was present in the Last PVC Ancestor, and most likely functional (see fig. 2 in the Pilhofer 2008 publication). So the very important question of "how do Planctomycetes divide, and in particular achieve the last steps of cytokinesis?".

This is the question that Jogler et a., 2102 Jbact address in their latest publication. Initial Phylogenetic analysis (Fig. 1)

provided a phylogenetic criterion to leave anammox bacteria out of our analysis

This is already important since it clearly splits the Planctomycetes in two group, the anammox on one side and all other non-anammox planctomycetes on the other. Anammox have been claimed to be early branching Planctomycetes and have particular biochemical reactions, endomembrane organization and dividing mode (most likely). Thus, it make sense to separate them from the other planctomycetes. This first analysis clearly puts them apart from the others.
The authors then go on to define the (non-anammox) planctomycetal core genome, by identifying those genes that have homologues in all selected genomes and discarding the ones that are also found in 'classical' bacteria such as E. coli and B. subtilis. They identified 114 clusters of exclusively planctomycetal proteins. No doubt that some of them should be related to the particular mode of division of those organisms. By example, one such cluster contain 39 membrane-coat like proteins that are structurally related to eukaryotic ones and likely to be involved in the membrane organisation in Planctomycetes (see Santarella-Mellwig et al., 2010 PLoS Biology,). Interestingly, a new FtsZ-like protein was recently described and found in a few Planctomycetes. However, Jogler et al. failed to detect homoloues in all other sequenced planctomycetes despite the use of a very similar strategy. Thus this FtsZ-like family might not be involved in division, at least not in all Planctomycetes.

They then provide an interesting analysis of the proteins found in this core planctomycetal genome and their domain composition.
One of the most interesting result is the finding that Planctomycetes are very poor in DNA-binding one-component systems (classical receptor-operator single proteins in bacteria, direct link between signal and output), but very rich in Ser/Thr protein kinases, which are common among eukaryotes and usually rare in bacteria. Again another striking relationship between those bacteria and eukaryotes.
They also found more two-components systems that are orphan genes, pointing toward a more complex regulation in planctomycetes.
But even more interesting, is their finding related to ECFs. ECFs are extracytoplasmic function sigma factors. In contrast to other bacteria, all planctomycetes are particularly rich in ECFs. Most planctomycetes ECFs can NOT be classified in the previously defined classes, which is probably just a reflexion of the bias towards model bacteria. G. obscuriglobus in particular is the second most ECF-rich bacteria, with the deltaproteobacterium Plesiocystis pacifica. They also identified a new class of ECFs that is specific to G. obscuriglobus. This class also contain more than half of the ECFs in the G. obscuriglobus genomes pointing to a recent evolution of those genes. Importantly, these are also the first membrane-anchored ECFs in bacteria. Given the conspicuous endomembrane organisation in this organism, it make sense that those proteins will play an important role in its regulation.

In conclusion, very interesting paper, even if not resolving the mystery of PVC division. On the other side, I would have found it interesting to do the same analysis on all PVC members. No doubt though that PVCs remains fascinating organisms, as this article beautifully illustrates.

Planctomycetes review

Fuerst and Sagulenko (Nature Review Microbiology 2011) present a nice review of the current knowledge of the Planctomycetes. They focus particularly on the genus Gemmata because of its endomembrane system seemingly surrounding the DNA, the presence of eukaryotic-like membrane coat proteins in its proteome and its capacity to do endocytosis. They conclude that:

"The compartmentalization of planctomycetes challenges our hypotheses regarding the origins of eukaryotic organelles."

This article nicely highlight the importance of studying other non-classical model of bacterial cell biology, like E. coli. There is also lots of phylogenetic interesting facts, evolution stimulating hints and questions are spread throughout the article.
They conclude with some hypothesis concerning the possible link between those bacteria and the origin of the eukaryotes, including convergent evolution, bacteria invention followed by LGT to the ancestral eukaryote, or LGT from the eukaryotes to the Planctomycetes and a complex LUCA. However, may be the strongest deduction is the following:

"Nevertheless, it seems clear that the planctomycetes are now a strong challenge to the idea that some form of fusion between archaeal and bacterial cells was necessary to evolve the eukaryote and its nucleus."

Whatever the correct answer, it is clear that Planctomycetes are fascinating bacteria that will keep us busy for the next couple of years. Keep watching!

Radiation tolerance

The Medalia team analyzed chromatin organization and radio resistance in the Planctomycetes Gemmata obscuriglobus. They report that Gemmata tolerates high doses of UV and ionizing radiation. Using cryoelectron tomography they found a highly ordered condensed-chromatin organization and a complex network of double membranes engulfing the condensed DNA. The complex double-membrane system emanates from the internal cell membrane. There is some ambiguity in the paper since on one side, they report that their results imply that the bacterial nucleoid is not completely sealed by the double-membrane system but on the other side, they conclude that multiple nucleoid domains are enclosed by the double-membrane system. So is it enclosed or not completely sealed?

The analysis of radio resistance is interesting. They report that G. obscuriglobus is highly resistant to UVC radiations. They suggest that this is linked to the condensed stated of the nucleoid and conclude that their observations support the notion that packed chromatin organization enhances radiation tolerance. Their tomography is based on a 15-nm-thick slice, when a typical bacteria is around 3 to 5 microns. When E. coli dies around 300 J/m2 of UV dose, Gemmata can support around 3 times that, close to 900 J/m2. This high level of radio resistance could be linked to non-homologuous DNA end joining (NHEJ), a phenomenon linked to double strand break repair, meiosis recombination and to the VDJ locus rearrangement processes in eukaryotes. Bioinformatics investigation of the Gemmata proteome revealed genes with homology to those for RecA, RecB, and RecD (no RecC), as well as for NHEJ mechanism ATP-dependent DNA ligases. Wittingly, they highlight that the G. obscuriglobus DNA repair ligase protein is significantly smaller than its bacterial homologues (58.4 vs >80kDa in other bacteria), suggesting that this lighter mass enhances the accessibility to the DNA breaks within the condensed DNA environment. Of course, the connection between higher radiation tolerance and DNA condensation is still to be demonstrated but the arguments and data presented here makes it very likely in this organism. Thus, G. obscuriglobus has evolved versatile mechanisms to deal with stress conditions.