Identification of Proteins Likely To Be Involved in Morphogenesis, Cell Division, and Signal Transduction in Planctomycetes by Comparative Genomics

Abstract

Members of the Planctomycetes clade share many unusual features for bacteria. Their cytoplasm contains membrane-bound compartments, they lack peptidoglycan and FtsZ, they divide by polar budding, and they are capable of endocytosis. Planctomycete genomes have remained enigmatic, generally being quite large (up to 9 Mb), and on average, 55% of their predicted proteins are of unknown function. Importantly, proteins related to the unusual traits of Planctomycetes remain largely unknown. Thus, we embarked on bioinformatic analyses of these genomes in an effort to predict proteins that are likely to be involved in compartmentalization, cell division, and signal transduction. We used three complementary strategies. First, we defined the Planctomycetes core genome and subtracted genes of well-studied model organisms. Second, we analyzed the gene content and synteny of morphogenesis and cell division genes and combined both methods using a "guilt-by-association" approach. Third, we identified signal transduction systems as well as sigma factors. These analyses provide a manageable list of candidate genes for future genetic studies and provide evidence for complex signaling in the Planctomycetes akin to that observed for bacteria with complex life-styles, such as Myxococcus xanthus.

Environmental Sensing in Actinobacteria: a Comprehensive Survey on the Signaling Capacity of This Phylum

“…This massive increase in sequence information significantly boosts the complexity of comparative genomics analyses but also facilitates grouping of previously unclassified proteins with similar characteristics, thereby enabling the generation of new hypotheses regarding their functions or mechanisms of action. This is reflected in the study by Jogler et al (32), in which the analysis of eight genome sequences of Planctomycetes resulted in the definition of eight new ECF groups, thereby classifying almost 80% of the Planctomycetes ECFs that could not be grouped by our original classification (6). The same was observed in the present study: the analysis of 119 actinobacterial genomes resulted in the identification of 18 new ECF groups.…”

“…The same was observed in the present study: the analysis of 119 actinobacterial genomes resulted in the identification of 18 new ECF groups. This allowed the classification of 81% of the actinobacterial ECFs that were not covered by any of the original ECF groups (5,6,32).…”

“…Among them, Ser/Thr kinases are the most common type (about 80% of all protein kinases). Bacterial Ser/Thr kinases, similarly to their eukaryotic counterparts, can phosphorylate a myriad of substrates and thereby structure complex signaling networks involved in diverse cellular processes, e.g., pathogenesis (27), cell division (28), control of gene expression (29), stress response (30), and quorum sensing (31) (32). While Actinobacteria are not as rich in protein kinases (with an average of only 2% of their 1CSs being protein kinases), some families are particularly protein kinase rich: Frankiaceae (5.5%), Actinomycetaceae (4.9%), Nocardiopsaceae (4.4%), Bifidobacteriaceae (4.2%), and Microbacteriaceae (3.1%).…”

Nested Bacterial Boxes: Nuclear and Other Intracellular Compartments in Planctomycetes

“…Correlated with internal compartment membranes, we might also expect unusual features of transport, regulation and signal transduction, and there is some indication of this from comparative genomics in several genera of planctomycetes including G. obscuriglobus [Jogler et al, 2012]. Planctomycetes display all three known signal transduction systems known in Bacteria, one-component systems (1CS), two-component systems (2CS) and the extracytoplasmic function system (ECF).…”

The 1st EMBO workshop on PVC bacteria—Planctomycetes–Verrucomicrobia–Chlamydiae superphylum: Exceptions to the bacterial definition?

“…This depends on development of genetic systems and Mareike Jogler of Christian Jogler's group (Leibniz Institute, DSMZ, Braunschweig, Germany) presented results indicating that, for the Planctomyces limnophilus model system, the use of GFP and translational fusions is close to being made useful as a tool for substantially accelerating the rate of progress in planctomycetes research. Comparative genomics by this group has also been a powerful tool for identifying putative genes involved in compartmentalization as well as cell division (Jogler et al 2012), and we can now move on to spatial localization of expressed protein fusions based on these genes to illuminate their exact function. This will be even more enhanced by correlation with EM studies using, for example, focused ion beam milling combined with cryoelectron tomography, as described by Marga Schüler (MPI Biochemistry, Germany).…”