The 1st EMBO workshop on PVC bacteria—Emphasis Ty

Authors: Damien P Devos Christian Jogler John A Fuerst

Publish Date: 2013/09/20

Volume: 104, Issue: 4, Pages: 443-449

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Abstract

The PVC superphylum is a phylogenetically supported collection of various related bacterial phyla that comprise unusual characteristics and traits The ‘PVC’ abbreviation derives from Planctomycetes Verrucomicrobia and Chlamydiae as members of this superphylum while additional bacterial phyla are related There has recently been increasing and exciting interest in the cell biology physiology and ecology of members of this superphylum including evolutionary implications of the complex cell organization of some species It is timely that international researchers in the PVC superphylum field met to discuss these developments The first meeting entirely dedicated to those bacteria the EMBO workshop “PVC superphylum Exceptions to the bacterial definition” was held at the Heidelberg University to catalyze the formation of a vital scientific community supporting PVCbacterial research More than 45 investigators from more than 20 countries PIs senior scientists and students attended the meeting and produced a great starting point for future collaborative research This Special Issue will focus on the EMBOPVC meeting This Perspective briefly summarizes the history of PVCresearch focusing on the key findings and provides a brief summary of the meeting with a focus on the major questions that arose during discussion and that might influence the research in the years to comeThe initially surprising grouping of bacteria with such different characteristics as ability to infect eukaryotic cells intracellularly in the case of members of the Chlamydiae and ability to oxidize ammonia in wastewater anaerobically in the case of anaerobic planctomycetes species is now amply supported Gupta et al 2012 Hou et al 2008 Kamneva et al 2010 Pilhofer et al 2008 Wagner and Horn 2006The PVC superphylum includes the phylum Planctomycetes a group of ubiquitous bacteria comprising both aerobic and anaerobic representatives that dwell in soil fresh water the oceans and most other locations in which microbial biodiversity has been analyzed Fuerst and Sagulenko 2011 the phylum Verrucomicrobia which includes a small number of species isolated from fresh water soil and human feces and by implication the gastrointestinal tract Derrien et al 2004 Hedlund et al 1997 the phylum Chlamydiae whose members are obligate intracellular pathogens the Poribacteria found so far only as obligate symbiont of sponges Fieseler et al 2004 the phylum Lentisphaerae which includes marine microorganisms and human gut microbiota Cho et al 2004 and the OP3 candidate phylum which contains no cultured representative but occurs in anoxic habitats Glöckner et al 2010 The inference that those organisms form a natural group was initially based on 16S rRNA phylogenetic analysis Wagner and Horn 2006 However since then it has been recovered by a range of further analyses and has become increasingly accepted as a valid taxonomic grouping Gupta et al 2012 Hou et al 2008 Kamneva et al 2010 Pilhofer et al 2008 Pol et al 2007 Fuerst 2013These bacteria have characteristics that set them apart from other bacteria and in some aspects resemble eukaryotes or archaea more than other bacteria For these reasons PVC superphylum members can be seen as exceptions within the domain Bacteria These exceptional features include a complex and dynamic endomembrane system with no equivalent in prokaryotes most clearly displayed in the phylum Planctomycetes but also in Verrucomicrobia and Lentisphaerae It also includes many other features such as tubulin in the case of some Verrucomicrobia sterols in the case of the planctomycete Gemmata obscuriglobus absence of peptidoglycan in planctomycetes where it is replaced by protein in the cell wall some verrucomicrobia and the chlamydiae so far as has been determined the lack in planctomycetes and chlamydiae of the otherwise ubiquitous FtsZ protein and FtsZdependent system for cell division widespread in all other bacteria presence of C1 transfer enzymes in many planctomycetes and the unique anaerobic ammoniumoxidizing metabolism in anammox planctomycetes Fuerst and Sagulenko 2011The PVC are not immune to controversy with different interpretations of the endomembrane organization the exact relation of the cell wall type in planctomycetes to that of Gramnegative bacteria with their outer membranes and the nature of the topology of the endomembranes which may envelop the nucleoid in some species especially of the planctomycete genus G obscuriglobus These controversies have in the wider evolutionary context been related to the question of whether eukaryotelike features in the PVC superphylum are evolutionarily homologous or analogous to those of domain Eukarya and Archaea members Devos 2012 Devos and Reynaud 2010 Forterre 2010 Forterre and Gribaldo 2010 Fuerst and Sagulenko 2011 McInerney et al 2011 Reynaud and Devos 2011Various PVC member species have applied relevance to areas extending from human health to wastewater remediation and understanding the global cycling of nitrogen Found in human gut some verrucomicrobia such as Akkermansia spp or some Lentisphaerae such as Victivallis spp van Passel et al 2011 might prove relevant to human health and prevention of human disease for example via the role of Akkermansia in mucin degradation in the intestine Derrien et al 2008 Everard et al 2013 Png et al 2010 The anammox species within the phylum Planctomycetes such as Kuenenia stuttgartiensis are of potential industrial interest since their ability to oxidize ammonia to molecular nitrogen is the basis of patented industrial processes for wastewater remediation reducing the excess nitrogen content of waste effluent improving effluent quality from sewage without the need for aeration and thus saving energy while sequestering carbon dioxide van Dongen et al 2001 Kartal et al 2010 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 2013The 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//wwwemboorg/fundingawards/coursesworkshops The small scale of the conference and of the community allowed for ample discussion between participants This issue is a compilation of a selection of the talks The full program can be found here http//eventsemboorg/13pvc/ A short summary of the sessions followsWithout any doubt the cell biology of planctomycetes is unique amongst bacteria and worth studying for new insights into the diversity of cell organization However while John Fuerst The University of Queensland Australia in his keynote introductory talk confirmed his earlier published demonstration of a nucleoidcontaining compartment in G obscuriglobus that resembles the eukaryotic nucleus using cryosubstitution electron microscopy freezefracture EM and reconstruction from serial sections as well as electron tomography Rachel SantarellaMellwig EMBL Germany in collaboration with Damien Devos Heidelberg University Germany presented a different view on G obscuriglobus’ cell biology emerging from thin sectioning and electron tomography that implies that such ‘compartment’ regions around the nucleoid may not be completely closed or surrounded by membranous envelopes SantarellaMellwig et al 2013 While both findings appear mutually exclusive they might be explained either by different stages of the G obscuriglobus life cycle nondividing versus dividing or by the different techniques used Future development of a synchronous division culture system may go towards resolving such apparent contradictions Both talks highlighted that further studies are required to ultimately define the spatial compartmentalization in G obscuriglobus during different stages in its life cycle In addition novel artifactfree imaging techniques were demonstrated in the talk of Marga Schüler MPI Germany While technically still challenging such techniques also have high potential to ultimately answer this question in the future

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