Genetic Analysis of the Upper Phenylacetate Catabolic Pathway in the Production of Tropodithietic Acid by Phaeobacter gallaeciensis

Berger, Martine; Brock, Nelson L.; Liesegang, Heiko; Dogs, Marco; Preuth, Ines; Simon, Meinhard; Dickschat, Jeroen S.; Brinkhoff, Thorsten

doi:10.1128/aem.07657-11

Cited by 52 publications

(61 citation statements)

References 51 publications

(64 reference statements)

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“…Our results show that TDA production in P. gallaeciensis is only modulated by the PgaI-PgaR QS system, and this indicates that QS is just one of several regulatory systems involved. This is in agreement with previous observations by Berger et al (35), who showed that pgaI and pgaR mutants are able to produce TDA in a minimal medium with phenylalanine as the sole carbon source. In some bacteria, the luxI-luxR QS system forms part of a hierarchically organized network where other regulators are integrated for the control of secondary-metabolite production (34,36), and this type of organization has been suggested previously for TDA production in P. gallaeciensis (35).…”

Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemssupporting

confidence: 83%

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Garcia

D’Alvise

Gram

2013

Appl Environ Microbiol

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Quorum sensing (QS) regulates Phaeobacter gallaeciensis antagonism in broth systems; however, we demonstrate here that QS is not important for antagonism in algal cultures. QS mutants reduced Vibrio anguillarum to the same extent as the wild type. Consequently, a combination of probiotic Phaeobacter and QS inhibitors is a feasible strategy for aquaculture disease control. Bacteria predominantly exist in mixed populations, and the behavior of the complete population is often affected by highly structured and sophisticated ways of communication.Many bacteria secrete small pheromone-like substances that allow the complete population to sense its density and subsequently alter, in a coordinated manner, gene expression. This type of communication between bacteria is known as quorum sensing (QS). QS systems play an important role in the regulation of genes related to virulence and, also, in genes involved in the production of bioactive compounds, such as antibiotics and enzymes (1-4).Roseobacter clade bacteria are some of the most common prokaryotes in oceanic and aquaculture environments (5-7). Some Roseobacter clade species, such as Phaeobacter gallaeciensis, Phaeobacter inhibens, and Ruegeria mobilis, produce a broad-spectrum antibacterial compound known as tropodithietic acid (TDA) (7-9). TDA does not induce resistance in the target organisms (10) and is the key compound for antagonism in laboratory broth cultures (11), in algae and rotifers, and in fish larval systems (12, 13). The ecological role of TDA is not known, but as TDA-producing bacteria can inhibit fish and shellfish pathogens, they have interesting prospects for application as probiotics in aquaculture (13,14).QS compounds of the acylated homoserine lactone (AHL) class are produced by some Roseobacter clade species (15-17), and TDA production is influenced by AHLs in Phaeobacter gallaeciensis. Genes homologous to the classical luxI (pgaI) and luxR (pgaR) genes have been identified, and a 24-h culture supernatant of a pgaI-negative mutant that is unable to produce the AHL compound did not antagonize other bacteria as the wild type did (18). Ruegeria mobilis does not produce AHLs, but in this bacterium, TDA itself can act as an autoinducer, controlling the expression of key genes for TDA production (19).Roseobacter bacteria are frequently associated with algae, both in oceanic waters and aquaculture systems (5, 7). In aquaculture, algae are used as a direct addition to fish larva-rearing tanks and to enrich live prey organisms, such as rotifers and Artemia, with fatty acids. Both algae and live feed have been suggested as vehicles for the introduction of probiotics into rearing systems (20,21), and a strategy of adding Phaeobacter strains to reduce pathogenic Vibrio in live feed and larval cultures has been proposed (12). As P. gallaeciensis antagonism is mainly caused by TDA and since TDA production is regulated by QS, we hypothesized that P. gallaeciensis antagonism in aquaculture settings (e.g., algal cultures) would also be affected by QS and, hence...

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Section: Antagonism Of P Gallaeciensis Qs Mutants In Broth Systemssupporting

confidence: 83%

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Garcia

D’Alvise

Gram

2013

Appl Environ Microbiol

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“…The taxonomic distribution of these chemolithotrophic gene sets does not map coherently to species phylogeny, suggesting that gain and loss of these traits have occurred multiple times during Roseobacter evolution, consistent with the scenario that roseobacters have continuously explored new ecological habitats. A few of these ecologically relevant genetic traits, including complete photosynthetic gene clusters (58), capabilities for production of the antibiotic tropodithietic acid (TDA) (59,60), and type IV secretion systems (61), are found on plasmids, suggesting that extrachromosomal DNA could be an important mechanism by which genes useful for environmental adaptation are transferred among roseobacters.…”

Section: Genome Contentmentioning

confidence: 99%

Evolutionary Ecology of the Marine Roseobacter Clade

Luo

Moran

2014

Microbiol Mol Biol Rev

260

239

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SUMMARY Members of the Roseobacter clade are equipped with a tremendous diversity of metabolic capabilities, which in part explains their success in so many different marine habitats. Ideas on how this diversity evolved and is maintained are reviewed, focusing on recent evolutionary studies exploring the timing and mechanisms of Roseobacter ecological diversification.

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“…TM1040 (Geng et al, 2008). The first enzyme of the phenylacetyl-CoA pathway paaK1 (phenylacetyl-CoA ligase) was shown to be non-essential for TDA production and this part of the pathway is probably substituted by conversion of phenylalanine via phenylpyruvate to phenylacetyl-CoA through the enzymatic action of either TyrB or HisC and Ior1 (Berger et al, 2012). Interruption of the plasmid-encoded paaZ2 gene, whose product mediates ring cleavage (Teufel et al, 2011), led to reduced TDA production.…”

Section: Tda Biosynthesis In P Gallaeciensis Dsm 17395mentioning

confidence: 99%

“…Among those is tdaA, which was shown to regulate the expression of tdaBEF and paaZ2 . The gene coding for the regulatory protein IorR (PGA1_c04480) is located adjacent to ior1 and was shown to be essential for the transcription of ior1 and the phenylalanine catabolism (Berger et al, 2012). The regulator PgaR (PGA1_c03880) is part of the PgaRI quorum-sensing system, which is essential for the transcription of tdaA .…”

Section: Tda Biosynthesis In P Gallaeciensis Dsm 17395mentioning

confidence: 99%

Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life

et al. 2012

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Phaeobacter gallaeciensis, a member of the abundant marine Roseobacter clade, is known to be an effective colonizer of biotic and abiotic marine surfaces. Production of the antibiotic tropodithietic acid (TDA) makes P. gallaeciensis a strong antagonist of many bacteria, including fish and mollusc pathogens. In addition to TDA, several other secondary metabolites are produced, allowing the mutualistic bacterium to also act as an opportunistic pathogen. Here we provide the manually annotated genome sequences of the P. gallaeciensis strains DSM 17395 and 2.10, isolated at the Atlantic coast of north western Spain and near Sydney, Australia, respectively. Despite their isolation sites from the two different hemispheres, the genome comparison demonstrated a surprisingly high level of synteny (only 3% nucleotide dissimilarity and 88% and 93% shared genes). Minor differences in the genomes result from horizontal gene transfer and phage infection. Comparison of the P. gallaeciensis genomes with those of other roseobacters revealed unique genomic traits, including the production of iron-scavenging siderophores. Experiments supported the predicted capacity of both strains to grow on various algal osmolytes. Transposon mutagenesis was used to expand the current knowledge on the TDA biosynthesis pathway in strain DSM 17395. This first comparative genomic analysis of finished genomes of two closely related strains belonging to one species of the Roseobacter clade revealed features that provide competitive advantages and facilitate surface attachment and interaction with eukaryotic hosts.

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Genetic Analysis of the Upper Phenylacetate Catabolic Pathway in the Production of Tropodithietic Acid by Phaeobacter gallaeciensis

Cited by 52 publications

References 51 publications

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Disruption of Cell-to-Cell Signaling Does Not Abolish the Antagonism of Phaeobacter gallaeciensis toward the Fish Pathogen Vibrio anguillarum in Algal Systems

Evolutionary Ecology of the Marine Roseobacter Clade

Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life

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