Identification of the Antibacterial Compound Produced by the Marine Epiphytic Bacterium Pseudovibrio sp. D323 and Related Sponge-Associated Bacteria

Penesyan, Anahit; Tebben, Jan; Lee, Matthew; Thomas, Torsten; Kjelleberg, Staffan; Harder, Tilmann; Egan, Suhelen

doi:10.3390/md9081391

Cited by 78 publications

(72 citation statements)

References 36 publications

(51 reference statements)

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“…TDA is also bactericidal against human pathogens including Salmonella enterica and Staphylococcus aureus (Porsby et al, 2011) and it has been recently been demonstrated that TDA acts by disrupting the proton motive force (Wilson et al, 2016). TDA is produced by R. mobilis, P. inhibens and Phaeobacter gallaeciensis, as well as by other alphaproteobacteria belonging to Pseudovibrio (Porsby et al, 2008;Geng and Belas, 2010;Penesyan et al, 2011;Harrington et al, 2014). Strains of Ruegeria and Phaeobacter produce TDA when grown under stagnant conditions in marine broth (MB) and TDA production coincides with bacterial rosette formation, a biofilm at the air-liquid interface, and production of a brown pigment that is an iron-TDA complex (Bruhn et al, 2007;Geng et al, 2008;Porsby et al, 2008;D'Alvise et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis

et al. 2016

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Tropodithietic acid (TDA)-producing Ruegeria mobilis strains of the Roseobacter clade have primarily been isolated from marine aquaculture and have probiotic potential due to inhibition of fish pathogens. We hypothesized that TDA producers with additional novel features are present in the oceanic environment. We isolated 42 TDA-producing R. mobilis strains during a global marine research cruise. While highly similar on the 16S ribosomal RNA gene level (99-100% identity), the strains separated into four sub-clusters in a multilocus sequence analysis. They were further differentiated to the strain level by average nucleotide identity using pairwise genome comparison. The four sub-clusters could not be associated with a specific environmental niche, however, correlated with the pattern of sub-typing using co-isolated phages, the number of prophages in the genomes and the distribution in ocean provinces. Major genomic differences within the sub-clusters include prophages and toxin-antitoxin systems. In general, the genome of R. mobilis revealed adaptation to a particle-associated life style and querying TARA ocean data confirmed that R. mobilis is more abundant in the particle-associated fraction than in the free-living fraction occurring in 40% and 6% of the samples, respectively. Our data and the TARA data, although lacking sufficient data from the polar regions, demonstrate that R. mobilis is a globally distributed marine bacterial species found primarily in the upper open oceans. It has preserved key phenotypic behaviors such as the production of TDA, but contains diverse sub-clusters, which could provide new capabilities for utilization in aquaculture.

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Section: Introductionmentioning

confidence: 99%

Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis

et al. 2016

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“…Pseudovibrio sp. D323, isolated from the red alga D. pulchra, produced tropodithietic acid, which inhibited the growth of other marine bacteria (Penesyan et al 2011). The authors speculated that tropodithietic acid prevents growth of competitors and inhibits growth of pathogens on the surface of the alga.…”

Section: Antibacterial Activity Heterotrophic Bacteriamentioning

confidence: 99%

Mini-review: Inhibition of biofouling by marine microorganisms

2013

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Any natural or artificial substratum exposed to seawater is quickly fouled by marine microorganisms and later by macrofouling species. Microfouling organisms on the surface of a substratum form heterogenic biofilms, which are composed of multiple species of heterotrophic bacteria, cyanobacteria, diatoms, protozoa and fungi. Biofilms on artificial structures create serious problems for industries worldwide, with effects including an increase in drag force and metal corrosion as well as a reduction in heat transfer efficiency. Additionally, microorganisms produce chemical compounds that may induce or inhibit settlement and growth of other fouling organisms. Since the last review by the first author on inhibition of biofouling by marine microbes in 2006, significant progress has been made in the field. Several antimicrobial, antialgal and antilarval compounds have been isolated from heterotrophic marine bacteria, cyanobacteria and fungi. Some of these compounds have multiple bioactivities. Microorganisms are able to disrupt biofilms by inhibition of bacterial signalling and production of enzymes that degrade bacterial signals and polymers. Epibiotic microorganisms associated with marine algae and invertebrates have a high antifouling (AF) potential, which can be used to solve biofouling problems in industry. However, more information about the production of AF compounds by marine microorganisms in situ and their mechanisms of action needs to be obtained. This review focuses on the AF activity of marine heterotrophic bacteria, cyanobacteria and fungi and covers publications from 2006 up to the end of 2012.

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“…T ropodithietic acid (TDA) is an antibacterial compound produced by members of the genera Ruegeria and Phaeobacter of the Roseobacter clade as well as by Pseudovibrio strains (Alphaproteobacteria) (1)(2)(3)(4). Several studies have focused on TDA-producing bacteria, especially as colonizers and symbionts of micro-and macroalgae (5)(6)(7)(8)(9) and as potential probiotics for marine aquaculture (10)(11)(12)(13)(14).…”

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confidence: 99%

Influence of Iron on Production of the Antibacterial Compound Tropodithietic Acid and Its Noninhibitory Analog in Phaeobacter inhibens

D’Alvise

Phippen

Nielsen

et al. 2016

Appl Environ Microbiol

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Tropodithietic acid (TDA) is an antibacterial compound produced by some Phaeobacter and Ruegeria spp. of the Roseobacter clade. TDA production is studied in marine broth or agar since antibacterial activity in other media is not observed. The purpose of this study was to determine how TDA production is influenced by substrate components. High concentrations of ferric citrate, as present in marine broth, or other iron sources were required for production of antibacterially active TDA. However, when supernatants of noninhibitory, low-iron cultures of Phaeobacter inhibens were acidified, antibacterial activity was detected in a bioassay. The absence of TDA in nonacidified cultures and the presence of TDA in acidified cultures were verified by liquid chromatography-high-resolution mass spectrometry. A noninhibitory TDA analog (pre-TDA) was produced by P. inhibens, Ruegeria mobilis F1926, and Phaeobacter sp. strain 27-4 under low-iron concentrations and was instantaneously converted to TDA when pH was lowered. Production of TDA in the presence of Fe 3؉ coincides with formation of a dark brown substance, which could be precipitated by acid addition. From this brown pigment TDA could be liberated slowly with aqueous ammonia, and both direct-infusion mass spectrometry and elemental analysis indicated a [Fe III (TDA) 2 ] x complex. The pigment could also be produced by precipitation of pure TDA with FeCl 3 . Our results raise questions about how biologically active TDA is produced in natural marine settings where iron is typically limited and whether the affinity of TDA to iron points to a physiological or ecological function of TDA other than as an antibacterial compound.T ropodithietic acid (TDA) is an antibacterial compound produced by members of the genera Ruegeria and Phaeobacter of the Roseobacter clade as well as by Pseudovibrio strains (Alphaproteobacteria) (1-4). Several studies have focused on TDA-producing bacteria, especially as colonizers and symbionts of micro-and macroalgae (5-9) and as potential probiotics for marine aquaculture (10-14). Thiotropocin, a tautomer of tropodithietic acid, was described as the antibiotic produced by a Pseudomonas species isolate from a Japanese soil sample (15, 16). A computational study has revealed that thiotropocin and tropodithietic acid exist as a pair of interconverting tautomers (17), and it has been speculated that thiotropocin was formed as an artifact from TDA during the p-bromobenzyl thioether derivatization used for its X-ray structure elucidation. To simplify matters, in the present study we refer to both compounds as TDA. The complete biosynthetic pathway of TDA has not been described; however, biosynthesis of TDA from glucose was investigated in a Pseudomonas sp., and shikimate and phenylpyruvate were identified as intermediate compounds (18). Twelve genes that are necessary for TDA production were found by random transposon mutagenesis in a Ruegeria (Silicibacter) sp. strain TM1040 (6), and a possible biosynthetic pathway has been suggested (19); however, the ...

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Identification of the Antibacterial Compound Produced by the Marine Epiphytic Bacterium Pseudovibrio sp. D323 and Related Sponge-Associated Bacteria

Cited by 78 publications

References 36 publications

Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis

Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis

Mini-review: Inhibition of biofouling by marine microorganisms

Influence of Iron on Production of the Antibacterial Compound Tropodithietic Acid and Its Noninhibitory Analog in Phaeobacter inhibens

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