The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance

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In the rRNA-based tree of life four bacterial phyla, comprising the Planctomycetes, Verrucomicrobia, Chlamydiae and Lentisphaerae, form together with the candidate phyla Poribacteria and OP3 a monophyletic group referred to as the PVC superphylum. This assemblage contains organisms that possess dramatically different lifestyles and which colonize sharply contrasting habitats. Some members of this group are among the most successful human pathogens, others are abundant soil microbes, and others still are of major importance for the marine nitrogen cycle and hold much promise for sustainable wastewater treatment. Recent comparative genomic and metagenomic analyses of a few representatives of this group revealed many unusual features and generated unexpected hypotheses regarding their physiology, some of which have already been confirmed experimentally. Furthermore, the availability of these genome sequences offered new insights into the evolutionary history of this peculiar group of microbes with major medical, ecological and biotechnological relevance.

Introduction

The most recent version of the bacterial tree of life consists of at least 50 phyla [1]. Owing to difficulties in the reconstruction of ancient relationships among bacterial phyla, however, their branching order in this tree remains largely unresolved. An interesting exception to this mistiness is the PVC superphylum — an assemblage of four bacterial phyla together with the Poribacteria and OP3 candidate phyla (which contain no cultured relatives), which is consistently recovered as a monophyletic group in 16S rRNA trees with different treeing methods (Figure 1). At first glance, this grouping is unexpected because no obvious similarities between the different phyla, which would reflect their shared evolutionary history, are apparent. Furthermore, bootstrap support for this superphylum is not very high (Figure 1) and there are a few reports in which some of its members do not cluster together [2, 3, 4]. However, owing to limited data at the time of their publication, these reports did not include all postulated phyla of the PVC superphylum, which might have resulted in biased tree topologies. Furthermore, a closer inspection of the available literature, including all recently published genome sequences of members of the PVC superphylum, reveals several unexpected similarities which lend additional support to the monophyly of this group. A better understanding of the evolution and biology of the bacteria of the PVC superphylum is of particular importance, because it encompasses organisms of major medical or environmental relevance. Furthermore, this grouping includes the recently discovered anaerobic ammonia oxidizers, which are increasingly exploited for the cost-effective removal of nitrogen compounds in sewage treatment.

The first part of this review summarizes separately for each phylum selected research highlights published since January 2004 (some earlier publications are also cited if required to provide context), while the second part aims to provide a synthesis of these findings in an evolutionary context.

Section snippets

Planctomycetes

Of all phyla grouped in the PVC superphylum, the Planctomycetes are most frequently represented in the current 16S rRNA Ribosomal Database Project (RDP) database (release 9.38) and make up ∼0.8% of all deposited sequences. This relatively low number has to be interpreted with caution, because the 16S rRNA genes of Planctomycetes do have mismatches to some PCR primers that are widely used in environmental diversity surveys [5]. Although this feature might lead to underrepresentation of the

Chlamydiae

In contrast to all other members of the PVC superphylum, the Chlamydiae have been studied extensively for decades. Chlamydiae are obligate intracellular bacteria characterized by an unique developmental cycle and, as such, are well-known pathogens of animals and humans. They cause several severe diseases such as trachoma, genital tract infections and pneumonia, with millions of infections reported each year. It was thus surprising that, in addition to the medically important chlamydiae (grouped

Verrucomicrobia

Verrucomicrobia are widely distributed and in the period reviewed here 16S rRNA sequences of members of this phylum were retrieved from various soils (e.g. see [56, 57]), confirming their importance in these systems. It has been estimated that Verrucomicrobia comprise upto 10% of the total bacteria in soil and contribute up to 9.8% of the bacterial 16S rRNA in these systems [58]. Although most members of this phylum remain uncultivated, Janssen's group recently isolated representatives of

Poribacteria, Lentisphaerae, the OP3 phylum and other environmental lineages

Poribacteria were detected in 2004 in marine demosponges and, to date, remain unknown from any other environmental niche [85]. No pure culture of Poribacteria is available but, according to specific fluorescence in situ hybridization analysis, they can occur in high numbers in these sponges. Furthermore, indirect evidence exists that Poribacteria, like Planctomycetes, possess a compartmented cytoplasm [85]. Recently, a 39 kb genomic fragment from an uncultured poribacterium was published [86].

Evolutionary history of the PVC superphylum

As discussed above, many members of the superphylum live in close association with eukaryotes and, for at least two phyla (Chlamydia and Poribacteria), no free-living members have been described. Therefore, it is tempting to speculate that the last common ancestor of the superphylum already possessed genes that could easily be modified to successfully colonize or invade eukaryotic hosts. First hints for possible candidates genes were obtained by extracting from all published genomes of

Conclusions

In conclusion, our understanding of the evolutionary history and biology of the Planctomycetes, the Chlamydiae, the Verrucomicrobia and their sister phyla has largely been propelled by genome and community genome analysis. The currently ongoing genome sequencing projects of Blastopirellula marina, Planctomyces maris, Gemmata obscuriglobus, Gemmata sp. strain Wa1-1 (Planctomycetes), Prosthecobacter dejongeii, Akkermansia muciniphila, Chthoniobacter flavus, Opitutus terrae, Verrucomicrobium sp.

Update

In April 2006 an interesting paper appeared that reports on the diversity and distribution of PVC superphylum members in the suboxic zone of the Black Sea [102]. This study also includes a phylogenetic tree which clusters Planctomycetes, Chlamydiae, Verrucomicrobia, Lentisphaerae and candidate phylum OP3, but does not display the Poribacteria.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors would like to express their gratitude to Mike Taylor for his critical comments on the manuscript. We would also like to thank Mike Jetten and Marc Strous (University of Nijmegen, Netherlands), Jean Weissenbach and Denis LePaslier (Genoscope, France), as well as Thomas Rattei and Werner Mewes (GSF, Germany) for great collaboration on this subject. Work in the authors’ laboratory is supported by the Austrian Science Fund (FWF) and the Federal Ministry for Education, Science and

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