Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea

Wagner‐Döbler, Irene; Rheims, Holger; Felske, Andreas; Pukall, Rüdiger; Tindall, Brian J.

doi:10.1099/ijs.0.02377-0

Cited by 78 publications

(23 citation statements)

References 56 publications

(46 reference statements)

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“…It displays 50% amino acid identity to Mesorhizobium loti RpoH-like sigma factor C, 47% identity to Bartonella quintana RpoH2, 46% identity to a Brucella melitensis 32 factor, and 42% identity to Sinorhizobium meliloti RpoH 2 (36,37). Together, R. sphaeroides RpoH II and RpoH I are most similar, displaying ϳ81% and ϳ84% amino acid identities, respectively, to the cognate RpoH proteins of two marine heterotrophs of the Roseobacter clade, Jannaschia helgolandensis (42) and Silicibacter pomeroyi (27). These values are consistent with a phylogenetic tree of 32 homologs (Fig.…”

Section: Resultsmentioning

confidence: 92%

Activity of Rhodobacter sphaeroides RpoH _II , a Second Member of the Heat Shock Sigma Factor Family

Green

Donohue

2006

J Bacteriol

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We have identified a second RpoH homolog, RpoH II , in the ␣-proteobacterium Rhodobacter sphaeroides. Primary amino acid sequence comparisons demonstrate that R. sphaeroides RpoH II belongs to a phylogenetically distinct group with RpoH orthologs from ␣-proteobacteria that contain two rpoH genes. Like its previously identified paralog, RpoH I , RpoH II is able to complement the temperature-sensitive phenotype of an Escherichia coli 32 (rpoH) mutant. In addition, we show that recombinant RpoH I and RpoH II each transcribe two E. coli 32 -dependent promoters (rpoD P HS and dnaK P1) when reconstituted with E. coli core RNA polymerase. We observed differences, however, in the ability of each sigma factor to recognize six R. sphaeroides promoters (cycA P1, groESL 1 , rpoD P HS , dnaK P1, hslO, and ecfE), all of which resemble the E. coli 32 promoter consensus. While RpoH I reconstituted with R. sphaeroides core RNA polymerase transcribed all six promoters, RpoH II produced detectable transcripts from only four promoters (cycA P1, groESL 1 , hslO, and ecfE). These results, in combination with previous work demonstrating that an RpoH I mutant mounts a typical heat shock response, suggest that while RpoH I and RpoH II have redundant roles in response to heat, they may also have roles in response to other environmental stresses.The ability to regulate gene expression through the use of alternate sigma factors enables bacteria to respond quickly to changes in the environment. These secondary sigma factors guide RNA polymerase to promoter elements whose target sequences differ from those of the primary sigma factors, thereby directing the transcription of a specific set of genes (44). One such rapid response to environmental perturbations, known as the heat shock response, uses an alternate sigma factor to increase the expression of proteins needed to maintain an intracellular milieu conducive for protein folding. While these heat-inducible gene products have traditionally been referred to as the heat shock proteins, increased heat shock protein expression is also induced by other stress conditions (11, 33). We are interested in alternate sigma factors that play a role in the heat shock or other stress responses of the ␣-proteobacterium Rhodobacter sphaeroides.In the ␥-proteobacterium Escherichia coli, 32 (encoded by rpoH) is the alternate sigma factor responsible for recognizing heat shock gene promoters (12). As a member of the 70 family of eubacterial sigma factors, 32 recognizes unique promoter sequences centered at positions Ϫ10 and Ϫ35 relative to the transcriptional start site (44). All 32 -like proteins are defined by a conserved region known as the "RpoH box"; they also contain conserved sequences in regions 2.4 and 4.2 that recognize the Ϫ10 and Ϫ35 elements, respectively, of heat shock promoters (29). While E. coli, with its single rpoH gene, sets the stage for much of what we know about bacterial heat shock regulation, several ␣-proteobacteria are known to encode multiple RpoH homologs. Three rpoH-like genes in...

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Section: Resultsmentioning

confidence: 92%

Activity of Rhodobacter sphaeroides RpoH _II , a Second Member of the Heat Shock Sigma Factor Family

Green

Donohue

2006

J Bacteriol

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“…We focused on the bacteriochlorophyll a containing type strains within the socalled Roseobacter clade. This is a heterogeneous group of organisms, representatives of which have been shown to have a high abundance in marine habitats (42,52). The strains studied were R. halodurans DSM15395 T , R. litoralis DSM6996 T , S. guttiformis DSM11458 T , and R. tolerans DSM11457 T .…”

Section: Resultsmentioning

confidence: 99%

Genome Organization and Localization of the pufLM Genes of the Photosynthesis Reaction Center in Phylogenetically Diverse Marine Alphaproteobacteria

Pradella

Allgaier

Hoch

et al. 2004

Appl Environ Microbiol

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Genome organization, plasmid content and localization of the pufLM genes of the photosynthesis reaction center were studied by pulsed-field gel electrophoresis (PFGE) in marine phototrophic Alphaproteobacteria. Both anaerobic phototrophs (Rhodobacter veldkampii and Rhodobacter sphaeroides) and strictly aerobic anoxygenic phototrophs from the Roseobacter-Sulfitobacter-Silicibacter clade (Roseivivax halodurans, Roseobacter litoralis, Staleya guttiformis, Roseovarius tolerans, and five new strains isolated from dinoflagellate cultures) were investigated. The complete genome size was estimated for R. litoralis DSM6996 T to be 4,704 kb, including three linear plasmids. All strains contained extrachromosomal elements of various conformations (linear or circular) and lengths (between 4.35 and 368 kb). In strain DFL-12, a member of a putative new genus isolated from a culture of the toxic dinoflagellate Prorocentrum lima, seven linear plasmids were found, together comprising 860 kb of genetic information. Hybridization with probes against the pufLM genes of the photosynthesis gene cluster after Southern transfer of the genomic DNAs showed these genes to be located on a linear plasmid of 91 kb in R. litoralis and on a linear plasmid of 120 kb in S. guttiformis, theoretically allowing their horizontal transfer. In all other strains, the pufLM genes were detected on the bacterial chromosome. The large number and significant size of the linear plasmids found especially in isolates from dinoflagellates might account for the metabolic versatility and presumed symbiotic association with eukaryotic hosts in these bacteria.

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“…They formed three subclusters, which were affiliated with recently described genera, i.e., Octadecabacter (13), isolated from arctic and antarctic ice; Marinosulfonomonas methylotropha (16); and J. helgolandensis from the North Sea (39). Even more similar to the third and largest cluster of SAR83-related sequences than J. helgolandensis were isolates obtained from dinoflagellate cultures (the DFL-12 cluster).…”

Section: Vol 69 2003 Photosynthesis In Roseobacter Marine Bacteria mentioning

confidence: 99%

“…Figure 1 shows that the isolates tended to form clusters of related organisms from the same habitat. These clusters were distributed over the whole Roseobacter clade and represented new genera (e.g., Jannaschia helgolandensis [39]) or species. Only in one case did a cluster contain a strain highly related, but not identical, to a strain which had been isolated from a different habitat: BIO-205, from biofilms in the cluster around HEL-45 from the water column.…”

Section: Vol 69 2003 Photosynthesis In Roseobacter Marine Bacteria mentioning

confidence: 99%

Aerobic Anoxygenic Photosynthesis in Roseobacter Clade Bacteria from Diverse Marine Habitats

Allgaier

Uphoff

Felske

et al. 2003

Appl Environ Microbiol

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129

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The marine Roseobacter clade comprises several genera of marine bacteria related to the uncultured SAR83 cluster, the second most abundant marine picoplankton lineage. Cultivated representatives of this clade are physiologically heterogeneous, and only some have the capability for aerobic anoxygenic photosynthesis, a process of potentially great ecological importance in the world's oceans. In an attempt to correlate phylogeny with ecology, we investigated the diversity of Roseobacter clade strains from various marine habitats (water samples, biofilms, laminariae, diatoms, and dinoflagellate cultures) by using the 16S rRNA gene as a phylogenetic marker gene. The potential for aerobic anoxygenic photosynthesis was determined on the genetic level by PCR amplification and sequencing of the pufLM genes of the bacterial photosynthesis reaction center and on the physiological level by detection of bacteriochlorophyll (Bchl) a. A collection of ca. 1,000 marine isolates was screened for members of the marine Roseobacter clade by 16S rRNA gene-directed multiplex PCR and sequencing. The 42 Roseobacter clade isolates found tended to form habitat-specific subclusters. The pufLM genes were detected in two groups of strains from dinoflagellate cultures but in none of the other Roseobacter clade isolates. Strains within the first group (the DFL-12 cluster) also synthesized Bchl a. Strains within the second group (the DFL-35 cluster) formed a new species of Roseovarius and did not produce Bchl a under the conditions investigated here, thus demonstrating the importance of genetic methods for screening of cultivation-dependent metabolic traits. The pufL genes of the dinoflagellate isolates were phylogenetically closely related to pufL genes from Betaproteobacteria, confirming similar previous observations which have been interpreted as indications of gene transfer events.Phototrophy through bacteriochlorophyll (Bchl) a-mediated aerobic anoxygenic photosynthesis (40) has been estimated (based on in situ measurements of Bchl a) to be responsible for as much as 5 to 10% of the energy generation in the upper layers of the tropical oceans (12,18,19). The bacteria responsible for the process are thought to be related to the uncultivated marine SAR83 cluster within the alpha subclass of the Proteobacteria, which represents the second most abundant lineage of marine picoplankton bacteria after SAR11 (2,11,29). However, aerobic phototrophs have also been found in other genera of Alphaproteobacteria (Erythrobacter, Roseivivax, and Sphingomonas) and Betaproteobacteria (Roseateles) as well as among as yet uncultivated marine bacteria (2). In recent years, a large number of bacteria which are distantly related to the SAR83 cluster, and which form the Roseobacter clade, have been cultivated. Presently, 12 genera are recognized within this clade: Ketogulonicigenium,

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Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea

Cited by 78 publications

References 56 publications

Activity of Rhodobacter sphaeroides RpoH _II , a Second Member of the Heat Shock Sigma Factor Family

Activity of Rhodobacter sphaeroides RpoH _II , a Second Member of the Heat Shock Sigma Factor Family

Genome Organization and Localization of the pufLM Genes of the Photosynthesis Reaction Center in Phylogenetically Diverse Marine Alphaproteobacteria

Aerobic Anoxygenic Photosynthesis in Roseobacter Clade Bacteria from Diverse Marine Habitats

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Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea

Cited by 78 publications

References 56 publications

Activity of Rhodobacter sphaeroides RpoH II , a Second Member of the Heat Shock Sigma Factor Family

Activity of Rhodobacter sphaeroides RpoH II , a Second Member of the Heat Shock Sigma Factor Family

Genome Organization and Localization of the pufLM Genes of the Photosynthesis Reaction Center in Phylogenetically Diverse Marine Alphaproteobacteria

Aerobic Anoxygenic Photosynthesis in Roseobacter Clade Bacteria from Diverse Marine Habitats

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Activity of Rhodobacter sphaeroides RpoH _II , a Second Member of the Heat Shock Sigma Factor Family

Activity of Rhodobacter sphaeroides RpoH _II , a Second Member of the Heat Shock Sigma Factor Family