Complete genome sequence of the myxobacterium Sorangium cellulosum

Abstract

The genus Sorangium synthesizes approximately half of the secondary metabolites isolated from myxobacteria, including the anti-cancer metabolite epothilone. We report the complete genome sequence of the model Sorangium strain S. cellulosum So ce56, which produces several natural products and has morphological and physiological properties typical of the genus. The circular genome, comprising 13,033,779 base pairs, is the largest bacterial genome sequenced to date. No global synteny with the genome of Myxococcus xanthus is apparent, revealing an unanticipated level of divergence between these myxobacteria. A large percentage of the genome is devoted to regulation, particularly post-translational phosphorylation, which probably supports the strain's complex, social lifestyle. This regulatory network includes the highest number of eukaryotic protein kinase-like kinases discovered in any organism. Seventeen secondary metabolite loci are encoded in the genome, as well as many enzymes with potential utility in industry.Natural products and their derivatives provide the basis for medicines targeting a wide range of human diseases. The Gram-negative myxobacteria, members of the d-subgroup of proteobacteria, are an important source of novel classes of secondary metabolites 1 . Of these, the genus Sorangium is particularly valuable, as 46% of metabolites isolated from myxobacteria 1 , including the potent antitumor compound epothilone 2 , derive from this group. The majority of myxobacterial metabolites are polyketides, nonribosomal polypeptides or hybrids of the two structures, many of which are synthesized on gigantic molecular assembly lines composed of polyketide synthase (PKS) and nonribosomal polypeptide synthetase (NRPS) multienzymes 3 . Sorangium strains exhibit additional characteristic features, including 'social behavior' , cell movement by gliding, biofilm formation and morphological differentiation culminating in complex multicellular structures called fruiting bodies 4 . Three myxobacterial suborders are known 5 and the availability of the genome sequence of Myxococcus xanthus (Cystobacterineae) 6 enables comparative analysis with the Sorangium cellulosum (Sorangiineae) genome to illuminate the basis for several important behavioral and metabolic differences. These include the ability of Sorangium strains to degrade complex plant materials (Fig. 1). S. cellulosum So ce56, an obligate aerobe, was established previously as a model Sorangium strain 7 by virtue of its favorable growth characteristics and ability to differentiate reproducibly under laboratory conditions. It synthesizes the cytotoxic chivosazoles 7 and the catecholate-type siderophores myxochelins 8 . Comparison of the complete genome sequence of strain S. cellulosum

Biogeography and phylogenetic diversity of a cluster of exclusively marine myxobacteria

“…The genome of S. cellulosum (account no. AM746676; Schneiker et al, 2007) contains two complete rRNA operons (16S-23S-5S), one incomplete (16S-23S) and one with two 5S rRNA genes (16S-23S-5S-5S).…”

“…In this complex, densitydependent life style, signalling compounds have a key role (Goldman et al, 2006), and myxobacteria are well known for the production of various secondary metabolites and thus are prime targets for the search of new secondary metabolites (Gerth et al, 2003;Wenzel and Mü ller, 2007;Weissman and Mü ller, 2010). They contain the largest genomes of all prokaryotes and the genome of Sorangium cellulosum, with 413 Mbp as the largest bacterial genome sequenced to date (Schneiker et al, 2007). Myxobacteria form a phylogenetically coherent group and constitute the order Myxococcales in the class Deltaproteobacteria.…”

Assessment of the bimodality in the distribution of bacterial genome sizes

“…It has, however, been speculated that species living in invariant niches tend to have small genomes, as stability acts to reduce genome size due the metabolic burden of replicating DNA with no adaptive value (Giovannoni et al, 2005(Giovannoni et al, , 2014 such as in obligatory and intracellular pathogens or mutualists (Moran, 2003;Klasson and Andersson, 2004;Moya et al, 2009). Due to their metabolic diversity, species with large genomes are potentially able to tackle a wider range of environmental conditions (Schneiker et al, 2007) and tend to be more ecologically successful where resources are scarce but diverse, and where there is little penalty for slow growth (Konstantinidis and Tiedje, 2004). The effect by which these two opposing evolutionary forces exert on the overall distribution of genome sizes was first observed by Koonin and Wolf in 2008, where it was reported that bacterial genome sizes show a bimodal distribution (Koonin and Wolf, 2008).…”

Complete genome sequence of the rifamycin SV-producing Amycolatopsis mediterranei U32 revealed its genetic characteristics in phylogeny and metabolism

“…This appears to be a common feature for the genus Amycolatopsis, because this circular topology was also suggested for the Amycolatopsis orientalis chromosome [14]. With a total length of 10 236 715 base pairs (bps) ( Table 1, GenBank accession number CP002000), the A. mediterranei genome is larger than that of S. coelicolor and S. erythraea, but smaller than that of the myxobacterium Sorangium cellulosum [15], and is apparently one of the largest prokaryotic genomes sequenced so far. The outer scale is numbered in megabases and indicates the core (red), quasi-core (orange), and non-core (sky blue).…”