Comparative Genomic Evidence for a Close Relationship between the Dimorphic Prosthecate Bacteria Hyphomonas neptunium and Caulobacter crescentus

Abstract

The dimorphic prosthecate bacteria (DPB) are ␣-proteobacteria that reproduce in an asymmetric manner rather than by binary fission and are of interest as simple models of development. Prior to this work, the only member of this group for which genome sequence was available was the model freshwater organism Caulobacter crescentus. Here we describe the genome sequence of Hyphomonas neptunium, a marine member of the DPB that differs from C. crescentus in that H. neptunium uses its stalk as a reproductive structure. Genome analysis indicates that this organism shares more genes with C. crescentus than it does with Silicibacter pomeroyi (a closer relative according to 16S rRNA phylogeny), that it relies upon a heterotrophic strategy utilizing a wide range of substrates, that its cell cycle is likely to be regulated in a similar manner to that of C. crescentus, and that the outer membrane complements of H. neptunium and C. crescentus are remarkably similar. H. neptunium swarmer cells are highly motile via a single polar flagellum. With the exception of cheY and cheR, genes required for chemotaxis were absent in the H. neptunium genome. Consistent with this observation, H. neptunium swarmer cells did not respond to any chemotactic stimuli that were tested, which suggests that H. neptunium motility is a random dispersal mechanism for swarmer cells rather than a stimulus-controlled navigation system for locating specific environments. In addition to providing insights into bacterial development, the H. neptunium genome will provide an important resource for the study of other interesting biological processes including chromosome segregation, polar growth, and cell aging.Unlike most bacteria, which reproduce by symmetric binary fission, dimorphic prosthecate bacteria (DPB) reproduce by asymmetric binary fission (e.g., Caulobacter crescentus) or budding (e.g., Hyphomonas and Hyphomicrobium species) to produce a motile swarmer cell from a nonmotile mother cell (68). The mother cell is distinguished by a presence of an appendage termed a prostheca or stalk (84), as well as generally having a holdfast that allows the cell to adhere to a surface (36). The swarmer cells, which are unable to reproduce, undergo a developmental process that results in their conversion to mother cells.The life cycle of DPB is analogous in many ways to that of dimorphic invertebrates, and this analogy is further supported by studies that have shown that the motile offspring of DPB, as in the multicellular case, are in a "juvenile" condition in which most energy is expended on motility and little on growth (26, 67). These facts suggest that DPB are good model systems for understanding the evolution and biology of dimorphic life in general.DPB are ubiquitous in both freshwater and marine environments but are found also to a lesser degree in soil (68). They are of considerable environmental interest since many Hyphomicrobium species can mineralize pollutants such as aromatic hydrocarbons (54), methyl chloride (34), and various alcohols, including metha...

Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum

“…Taxonomic affiliations of the predicted protein sequences derived from this contig were assigned using the Automated Phylogenetic Inference System software (APIS) (42), which generates a phylogenetic tree for each ORF in a genomic or metagenomic sample using homologous proteins from complete genomes. APIS classifies each ORF taxonomically and functionally based on phylogenetic position.…”

“…The 16S rRNA gene had a top BLAST hit to a member of TM6. Taxonomic affiliations of the predicted protein sequences derived from this contig were also assigned using APIS (42). APIS generates a phylogenetic tree for each ORF in a genomic or metagenomic sample using homologous proteins from PhyloDB 1.05, a J. Craig Venter Institute database containing proteins from all publically available complete genomes as of August 15, 2012.…”

The BAM complex subunit BamE (SmpA) is required for membrane integrity, stalk growth and normal levels of outer membrane β-barrel proteins in Caulobacter crescentus

“…However, proteins closely related to CC1365 encoded in other a-proteobacterial genomes have been annotated as members of the SmpA/OmlA family of lipoproteins (Badger et al, 2006;DelVecchio et al, 2002), which is present in the alpha-, beta-and gammaproteobacteria. We aligned the amino acid sequence of CC1365 with BamE and OmlA proteins that have been studied experimentally from the organisms E. coli (Sklar et al, 2007), Salmonella enterica serovar Typhimurium (Lewis et al, 2008), P. aeruginosa PAO1 (Ochsner et al, 1999) and Xanthomonas axonopodis pv.…”

Hellea balneolensis gen. nov., sp. nov., a prosthecate alphaproteobacterium from the Mediterranean Sea

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