Inactivation of
            <i>Vibrio anguillarum</i>
            by Attached and Planktonic
            <i>Roseobacter</i>
            Cells

D’Alvise, Paul; Melchiorsen, Jette; Porsby, Cisse Hedegaard; Nielsen, Kristian Fog; Gram, Lone

doi:10.1128/aem.02717-09

Cited by 54 publications

(66 citation statements)

References 40 publications

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“…To reduce the use of antibiotics, we and others have focused on use of probiotic strategies and used bacteria of the Roseobacter clade that can antagonize fish-pathogenic bacteria without harming the fish or their live feed (D'Alvise et al, 2012(D'Alvise et al, , 2013. Specifically, strains belonging to the species Ruegeria mobilis and Phaeobacter inhibens are potent antagonists of the fish pathogens (Planas et al, 2006;Porsby et al, 2008;D'Alvise et al, 2010) primarily caused by production of the antibacterial compound tropodithietic acid (TDA) (D'Alvise et al, 2010(D'Alvise et al, , 2012. 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).…”

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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“…Several co‐culture studies of P. inhibens and V. anguillarum in axenic systems have shown significant inhibition of vibrios, resulting in lowered vibrio counts relative to the inoculum level (D'Alvise et al ., 2010, 2012; Grotkjær et al ., 2016b). In contrast, P. inhibens kept V. anguillarum at the inoculum level in both the non‐axenic co‐culture experiments conducted in the present study and in similar experiments with non‐axenic Tetraselmis and Artemia (Grotkjær et al ., 2016a).…”

Section: Discussionmentioning

confidence: 99%

Effect of TDA‐producing Phaeobacter inhibens on the fish pathogen Vibrio anguillarum in non‐axenic algae and copepod systems

Rasmussen

Erner

Bentzon-Tilia

et al. 2018

Microbial Biotechnology

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SummaryThe expanding aquaculture industry plays an important role in feeding the growing human population and with the expansion, sustainable bacterial disease control, such as probiotics, becomes increasingly important. Tropodithietic acid (TDA)‐producing Phaeobacter spp. can protect live feed, for example rotifers and Artemia as well as larvae of turbot and cod against pathogenic vibrios. Here, we show that the emerging live feed, copepods, is unaffected by colonization of the fish pathogen Vibrio anguillarum, making them potential infection vectors. However, TDA‐producing Phaeobacter inhibens was able to significantly inhibit V. anguillarum in non‐axenic cultures of copepod Acartia tonsa and the copepod feed Rhodomonas salina. Vibrio grew to 106 CFU ml−1 and 107 CFU ml−1 in copepod and R. salina cultures, respectively. However, vibrio counts remained at the inoculum level (104 CFU ml−1) when P. inhibens was also added. We further developed a semi‐strain‐specific qPCR for V. anguillarum to detect and quantify the pathogen in non‐axenic systems. In conclusion, P. inhibens efficiently inhibits the fish larval pathogen V. anguillarum in the emerging live feed, copepods, supporting its use as a probiotic in aquaculture. Furthermore, qPCR provides an effective method for detecting vibrio pathogens in complex non‐axenic live feed systems.

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“…It was previously shown that TDA-producing Roseobacter species have the ability to inhibit or kill other marine bacteria (3,13,22,41) and that purified TDA alone has a growth-inhibitory effect on marine bacteria (3). This study shows that TDA is a broad-spectrum antibacterial compound effective against all the human-pathogenic strains tested, in- Typhimurium strain harboring acrB, which encodes a multidrug efflux pump.…”

Section: Discussionmentioning

confidence: 99%

“…The killing or inhibitory effect is related to TDA production (3,22,41). Thus, D'Alvise et al previously showed that the fish-pathogenic bacterium Vibrio anguillarum strain 90-11-287 was killed only by TDA-producing wild-type Phaeobacter strain 27-4 and not by a mutant deficient in TDA production (13).…”

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Resistance and Tolerance to Tropodithietic Acid, an Antimicrobial in Aquaculture, Is Hard To Select

Porsby

Webber

Nielsen

et al. 2011

Antimicrob Agents Chemother

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The antibacterial compound tropodithietic acid (TDA) is produced by bacteria of the marine Roseobacter clade and is thought to explain the fish probiotic properties of some roseobacters. The aim of the present study was to determine the antibacterial spectrum of TDA and the likelihood of development of TDA resistance. A bacterial extract containing 95% TDA was effective against a range of human-pathogenic bacteria, including both Gram-negative and Gram-positive bacteria. TDA was bactericidal against Salmonella enterica serovar Typhimurium SL1344 and Staphylococcus aureus NCTC 12493 and killed both growing and nongrowing cells. Several experimental approaches were used to select mutants resistant to TDA or subpopulations of strains with enhanced tolerance to TDA. No approach (single exposures to TDA extract administered via different methods, screening of a transposon library for resistant mutants, or prolonged exposure to incremental concentrations of TDA) resulted in resistant or tolerant strains. After more than 300 generations exposed to sub-MIC and MIC concentrations of a TDA-containing extract, strains tolerant to 2؋ the MIC of TDA for wild-type strains were selected, but the tolerance disappeared after one passage in medium without TDA extract. S. Typhimurium mutants with nonfunctional efflux pump and porin genes had the same TDA susceptibility as wild-type strains, suggesting that efflux pumps and porins are not involved in innate tolerance to TDA. TDA is a promising broad-spectrum antimicrobial in part due to the fact that enhanced tolerance is difficult to gain and that the TDA-tolerant phenotype appears to confer only low-level resistance and is very unstable.

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Inactivation of Vibrio anguillarum by Attached and Planktonic Roseobacter Cells

Cited by 54 publications

References 40 publications

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

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

Effect of TDA‐producing Phaeobacter inhibens on the fish pathogen Vibrio anguillarum in non‐axenic algae and copepod systems

Resistance and Tolerance to Tropodithietic Acid, an Antimicrobial in Aquaculture, Is Hard To Select

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