From genome mining to phenotypic microarrays: Planctomycetes as source for novel bioactive molecules

Abstract

Most members of the phylum Planctomycetes share many unusual traits that are unique for bacteria, since they divide independent of FtsZ through asymmetric budding, possess a complex life cycle and comprise a compartmentalized cell plan. Besides their complex cell biological features Planctomycetes are environmentally important and play major roles in global matter fluxes. Such features have been successfully employed in biotechnological applications such as the anaerobic oxidation of ammonium in wastewater treatment plants or the utilization of enzymes for biotechnological processes. However, little is known about planctomycetal secondary metabolites. This is surprising as Planctomycetes have several key features in common with known producers of small bioactive molecules such as Streptomycetes or Myxobacteria: a complex life style and large genome sizes. Planctomycetal genomes with an average size of 6.9 MB appear as tempting targets for drug discovery approaches. To enable the hunt for bioactive molecules from Planctomycetes, we performed a comprehensive genome mining approach employing the antiSMASH secondary metabolite identification pipeline and found 102 candidate genes or clusters within the analyzed 13 genomes. However, as most genes and operons related to secondary metabolite production are exclusively expressed under certain environmental conditions, we optimized Phenotype MicroArray protocols for Rhodopirellula baltica and Planctomyces limnophilus to allow high throughput screening of putative stimulating carbon sources. Our results point towards a previously postulated relationship of Planctomycetes with algae or plants, which secrete compounds that might serve as trigger to stimulate the secondary metabolite production in Planctomycetes. Thus, this study provides the necessary starting point to explore planctomycetal small molecules for drug development.

Characterization of a Planctomycetal Organelle: a Novel Bacterial Microcompartment for the Aerobic Degradation of Plant Saccharides

“…Recently, a comprehensive metabolic screen of P. limnophilus suggested that the organism is specialized to degrade plant-derived sugars and polysaccharides (62). Our results confirmed these observations and further implicated the involvement of the BMC in degrading some of these compounds.…”

“…The propanediol is produced as a result of cofactor recycling and may be excreted; there is no obvious evidence of P. limnophilus being able to metabolize this compound (see Fig. S5 in the supplemental material, PM1 well D4), an observation corroborated by other investigators (62). Due to the PV BMC metabolism being aerobic, the end products of the BMC metabolism (DHAP and/or pyruvate) likely enter the tricarboxylic acid (TCA) cycle and generate ATP through oxidative phosphorylation.…”

“…Planctomycetes have been shown to attach to detritus (marine snow), which is composed of decaying plant and animal materials that most likely contain L-fucose and L-rhamnose, and are thought to be involved in carbon cycling in oceans (76). Furthermore, a recent study has shown that two planctomycetes, one marine and one freshwater, are capable of degrading several other plant-derived sugars (62). Seaweeds and other marine algae contain an abundance of sulfated polysaccharides (77), two of which are fucoidan and ulvan, which are composed of 95% L-fucose (53) and 55% L-rhamnose (75), respectively.…”

Planctomycetes and macroalgae, a striking association

“…These authors also verified in R. baltica SH1 T sulphatase expression profiles in cells grown on different sulfated polysaccharides. Polysaccharide utilization was also confirmed by the work of Jeske et al (2013) where R. baltica was checked for potential utilization of several polymers. It was able to utilize laminarin, mannitol, pectin, chondroitin sulfate, N-acetylgalactosamine, and D-glucuronic acid.…”

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

“…This process is also critical to operation of the global nitrogen cycle, producing much of the nitrogen in the air we breathe via anaerobic ammonium recycling in environments such as the ocean's oxygen minimum zones (Kalvelage et al 2011). As a unique divergent unexplored group of bacteria, planctomycetes are an emerging source of novel secondary metabolites, which very well might be useful for drug development (Jeske et al 2013 The first meeting dedicated to these bacteria took place in early March 2013 at the Heidelberg University, thanks to a generous donation from the EMBO Courses and Workshops program (http://www.embo. org/funding-awards/courses-workshops).…”