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Peter D. Steinberg - One of the best experts on this subject based on the ideXlab platform.
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Interactions within the microbiome alter microbial interactions with host chemical defences and affect disease in a marine holobiont.
Scientific Reports, 2019Co-Authors: Sharon R. Longford, Staffan Kjelleberg, Alexandra H. Campbell, Shaun Nielsen, Rebecca J. Case, Peter D. SteinbergAbstract:Our understanding of diseases has been transformed by the realisation that people are holobionts, comprised of a host and its associated microbiome(s). Disease can also have devastating effects on populations of marine organisms, including dominant habitat formers such as seaweed holobionts. However, we know very little about how interactions between microorganisms within microbiomes - of humans or marine organisms – affect host health and there is no underpinning theoretical framework for exploring this. We applied ecological models of succession to bacterial communities to understand how interactions within a seaweed microbiome affect the host. We observed succession of surface microbiomes on the red seaweed Delisea pulchra in situ, following a disturbance, with communities ‘recovering’ to resemble undisturbed states after only 12 days. Further, if this recovery was perturbed, a bleaching disease previously described for this seaweed developed. Early successional strains of bacteria protected the host from colonisation by a pathogenic, later successional strain. Host chemical defences also prevented disease, such that within-microbiome interactions were most important when the host’s chemical defences were inhibited. This is the first experimental evidence that interactions within microbiomes have important implications for host health and disease in a dominant marine habitat-forming organism.
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SYMPOSIUM Interfaces Between Bacterial and Eukaryotic ‘‘Neuroecology’’
2016Co-Authors: Peter D. Steinberg, Scott A Rice, Diane Mcdougald, Ra H. Campbell, Tilmann HarderAbstract:Synopsis The sensory capacity of bacteria and macroalgae (seaweeds) is limited with respect to many modalities (visual, auditory) common in ‘‘higher’ ’ organisms such as animals. Thus, we expect that other modalities, such as chemical signaling and sensing, would play particularly important roles in their sensory ecology. Here, we discuss two examples of chemical signaling in bacteria and seaweeds: (1) the role of chemical defenses and quorum-sensing (QS) regulatory systems in bacterial colonization and infection of the red alga Delisea pulchra and their ecological consequences, and (2) the regulation of dispersal and differentiation by nitric oxide (NO) in bacterial biofilms. Consistent with the goals of neuroecology, in both cases, we investigate the links between specific signal-mediated molecular mechanisms, and eco-logical outcomes, for populations or assemblages of bacteria or seaweeds. We conclude by suggesting that because of the fundamental role played by chemical signaling in bacteria, bacterial systems, either by themselves or in interactions with other organisms, have much to offer for understanding general issues in neuroecology. Thus, further integration of microbiology with the biology of eukaryotes would seem warranted and is likely to prove illuminating
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Expanding our Understanding of the Seaweed Holobiont: RNA Viruses of the Red Alga Delisea pulchra
Frontiers in Microbiology, 2016Co-Authors: Tim Lachnit, Torsten Thomas, Peter D. SteinbergAbstract:Marine seaweeds are holobionts comprised of the macroalgal hosts and their associated microbiota. While the composition of the bacterial component of seaweed microbiomes is increasingly studied, almost nothing is known about the presence, diversity and composition of viruses in macroalgae in situ. In this study, we characterise for the first time the viruses associated with a red macroalga, Delisea pulchra. Using transmission electron microscopy we identified diverse morphotypes of virus-like particles in D. pulchra ranging from icosahedral to bacilliform to coiled pleomorphic as well as bacteriophages. Virome sequencing revealed the presence of a diverse group of dsRNA viruses affiliated to the genus Totivirus, known to infect plant pathogenic fungi. We further identified a ssRNA virus belonging to the order Picornavirales with a close phylogenetic relationship to a pathogenic virus infecting marine diatoms. The results of this study shed light on a so far neglected part of the seaweed holobiont, and suggest that some of these may be possible pathogens for a host that is already known to be significantly impacted by bacterial infections.
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Community Structure and Functional Gene Profile of Bacteria on Healthy and Diseased Thalli of the Red Seaweed Delisea pulchra
PLoS ONE, 2012Co-Authors: Neil D. Fernandes, Peter D. Steinberg, Staffan Kjelleberg, Doug Rusch, Torsten ThomasAbstract:Disease is increasingly viewed as a major factor in the ecology of marine communities and its impact appears to be increasing with environmental change, such as global warming. The temperate macroalga Delisea pulchra bleaches in Southeast Australia during warm summer periods, a phenomenon which previous studies have indicated is caused by a temperature induced bacterial disease. In order to better understand the ecology of this disease, the bacterial communities associated with threes type of samples was investigated using 16S rRNA gene and environmental shotgun sequencing: 1) unbleached (healthy) D. pulchra 2) bleached parts of D. pulchra and 3) apparently healthy tissue adjacent to bleached regions. Phylogenetic differences between healthy and bleached communities mainly reflected relative changes in the taxa Colwelliaceae, Rhodobacteraceae, Thalassomonas and Parvularcula. Comparative metagenomics showed clear difference in the communities of healthy and diseased D. pulchra as reflected by changes in functions associated with transcriptional regulation, cation/multidrug efflux and non-ribosomal peptide synthesis. Importantly, the phylogenetic and functional composition of apparently healthy tissue adjacent to bleached sections of the thalli indicated that changes in the microbial communities already occur in the absence of visible tissue damage. This shift in unbleached sections might be due to the decrease in furanones, algal metabolites which are antagonists of bacterial quorum sensing. This study reveals the complex shift in the community composition associated with bleaching of Delisea pulchra and together with previous studies is consistent with a model in which elevated temperatures reduce levels of chemical defenses in stressed thalli, leading to colonization or proliferation by opportunistic pathogens or scavengers.
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Chemical Mediation of Ternary Interactions Between Marine Holobionts and Their Environment as Exemplified by the Red Alga Delisea pulchra
Journal of Chemical Ecology, 2012Co-Authors: Tilmann Harder, Suhelen Egan, Alexandra H. Campbell, Peter D. SteinbergAbstract:The need for animals and plants to control microbial colonization is important in the marine environment with its high densities of microscopic propagules and seawater that provides an ideal medium for their dispersal. In contrast to the traditional emphasis on antagonistic interactions of marine organisms with microbes, emerging studies lend support to the notion that health and performance of many marine organisms are functionally regulated and assisted by associated microbes, an ecological concept defined as a holobiont. While antimicrobial activities of marine secondary metabolites have been studied in great depth ex-situ , we are beginning to understand how some of these compounds function in an ecological context to maintain the performance of marine holobionts. The present article reviews two decades of our research on the red seaweed Delisea pulchra by addressing: the defense chemistry of this seaweed; chemically-mediated interactions between the seaweed and its natural enemies; and the negative influence of elevated seawater temperature on these interactions. Our understanding of these defense compounds and the functional roles they play for D. pulchra extends from molecular interactions with bacterial cell signaling molecules, to ecosystem-scale consequences of chemically-controlled disease and herbivory. Delisea pulchra produces halogenated furanones that antagonize the same receptor as acylated homoserine lactones (AHL)—a group of widespread intercellular communication signals among bacteria. Halogenated furanones compete with and inhibit bacterial cell-to-cell communication, and thus interfere with important bacterial communication-regulated processes, such as biofilm formation. In a predictable pattern that occurs at the ecological level of entire populations, environmental stress interferes with the production of halogenated furanones, causing downstream processes that ultimately result in disease of the algal holobiont.
Staffan Kjelleberg - One of the best experts on this subject based on the ideXlab platform.
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Interactions within the microbiome alter microbial interactions with host chemical defences and affect disease in a marine holobiont.
Scientific Reports, 2019Co-Authors: Sharon R. Longford, Staffan Kjelleberg, Alexandra H. Campbell, Shaun Nielsen, Rebecca J. Case, Peter D. SteinbergAbstract:Our understanding of diseases has been transformed by the realisation that people are holobionts, comprised of a host and its associated microbiome(s). Disease can also have devastating effects on populations of marine organisms, including dominant habitat formers such as seaweed holobionts. However, we know very little about how interactions between microorganisms within microbiomes - of humans or marine organisms – affect host health and there is no underpinning theoretical framework for exploring this. We applied ecological models of succession to bacterial communities to understand how interactions within a seaweed microbiome affect the host. We observed succession of surface microbiomes on the red seaweed Delisea pulchra in situ, following a disturbance, with communities ‘recovering’ to resemble undisturbed states after only 12 days. Further, if this recovery was perturbed, a bleaching disease previously described for this seaweed developed. Early successional strains of bacteria protected the host from colonisation by a pathogenic, later successional strain. Host chemical defences also prevented disease, such that within-microbiome interactions were most important when the host’s chemical defences were inhibited. This is the first experimental evidence that interactions within microbiomes have important implications for host health and disease in a dominant marine habitat-forming organism.
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Community Structure and Functional Gene Profile of Bacteria on Healthy and Diseased Thalli of the Red Seaweed Delisea pulchra
2016Co-Authors: Neil Fern, Staffan Kjelleberg, Peter Steinberg, Doug Rusch, Torsten ThomasAbstract:Disease is increasingly viewed as a major factor in the ecology of marine communities and its impact appears to be increasing with environmental change, such as global warming. The temperate macroalga Delisea pulchra bleaches in Southeast Australia during warm summer periods, a phenomenon which previous studies have indicated is caused by a temperature induced bacterial disease. In order to better understand the ecology of this disease, the bacterial communities associated with threes type of samples was investigated using 16S rRNA gene and environmental shotgun sequencing: 1) unbleached (healthy) D. pulchra 2) bleached parts of D. pulchra and 3) apparently healthy tissue adjacent to bleached regions. Phylogenetic differences between healthy and bleached communities mainly reflected relative changes in the taxa Colwelliaceae, Rhodobacteraceae, Thalassomonas and Parvularcula. Comparative metagenomics showed clear difference in the communities of healthy and diseased D. pulchra as reflected by changes in functions associated with transcriptional regulation, cation/multidrug efflux and non-ribosomal peptide synthesis. Importantly, the phylogenetic and functional composition of apparently healthy tissue adjacent to bleached sections of the thalli indicated that changes in the microbial communities already occur in the absence of visible tissue damage. This shift in unbleached sections might be due to the decrease in furanones, algal metabolites which are antagonists of bacterial quorum sensing. This study reveals the complex shift in the community composition associated with bleaching of Delisea pulchra and together with previou
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Multiple opportunistic pathogens can cause a bleaching disease in the red seaweed Delisea pulchra.
Environmental Microbiology, 2016Co-Authors: Vipra Kumar, Torsten Thomas, Staffan Kjelleberg, Enrique Zozaya‐valdés, Suhelen EganAbstract:While macroalgae (or seaweeds) are increasingly recognized to suffer from disease, in most cases the causative agents are unknown. The model macroalga Delisea pulchra is susceptible to a bleaching disease and previous work has identified two epiphytic bacteria, belonging to the Roseobacter clade, that cause bleaching under laboratory conditions. However, recent environmental surveys have shown that these in vitro pathogens are not abundant in naturally bleached D. pulchra, suggesting the presence of other pathogens capable of causing this algal disease. To test this hypothesis, we cultured bacteria that were abundant on bleached tissue across multiple disease events and assessed their ability to cause bleaching disease. We identified the new pathogens Alteromonas sp. BL110, Aquimarina sp. AD1 and BL5 and Agarivorans sp BL7 that are phylogenetically diverse, distinct from the previous two pathogens and can also be found in low abundance in healthy individuals. Moreover, we found that bacterial communities of diseased individuals that were infected with these pathogens were less diverse and more divergent from each other than those of healthy algae. This study demonstrates that multiple and opportunistic pathogens can cause the same disease outcome for D. pulchra and we postulate that such pathogens are more common in marine systems than previously anticipated.
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VarR controls colonization and virulence in the marine macroalgal pathogen Nautella italica R11
Frontiers in Microbiology, 2015Co-Authors: Melissa Gardiner, Torsten Thomas, Staffan Kjelleberg, Neil D. Fernandes, Dennis Nowakowski, Mark J. Raftery, Ling Zhong, Suhelen EganAbstract:There is increasing evidence to suggest that macroalgae (seaweeds) are susceptible to infectious disease. However, to date, little is known about the mechanisms that facilitate the colonization and virulence of microbial seaweed pathogens. One well-described example of a seaweed disease is the bleaching of the red alga Delisea pulchra, which can be caused by the bacterium Nautella italica R11, a member of the Roseobacter clade. This pathogen contains a unique luxR-type gene, varR, which we hypothesize controls its colonization and virulence. We show here that a varR knock-out strain is deficient in its ability to cause disease in D. pulchra and is defective in biofilm formation and attachment to a common algal polysaccharide. Moreover complementation of the varR gene in trans can restore these functions to the wild type levels. Proteomic analysis of bacterial cells in planktonic and biofilm growth highlight the potential importance of nitrogen scavenging, mobilization of energy reserves, and stress resistance in the biofilm lifestyle of N. italica R11. Moreover, we show that VarR regulates the expression of a specific subset of biofilm-associated proteins. Taken together these data suggest that VarR controls colonization and persistence of N. italica R11 on the surface of a macroalgal host and that it is an important regulator of virulence.
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Printed in Great Britain
2013Co-Authors: Michael Manefield, Rocky De N~s, Roger Read, Peter Steinbergf, Staffan Kjelleberg, Sciences* Centre ForAbstract:Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protei
Suhelen Egan - One of the best experts on this subject based on the ideXlab platform.
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Comparative genome analysis provides novel insight into the interaction of Aquimarina sp. AD1, BL5 and AD10 with their macroalgal host.
Marine Genomics, 2019Co-Authors: Jennifer Hudson, Vipra Kumar, Suhelen EganAbstract:Abstract The Aquimarina genus is widely distributed throughout the marine environment, however little is understood regarding its ecological role, particularly when in association with eukaryotic hosts. Here, we examine the genomes of two opportunistic pathogens, Aquimarina sp. AD1 and BL5, and a non-pathogenic strain Aquimarina sp. AD10, that were isolated from diseased individuals of the red alga Delisea pulchra. Each strain encodes multiple genes for the degradation of marine carbohydrates and vitamin biosynthesis. These traits are hypothesised to promote nutrient exchange between the Aquimarina strains and their algal host, facilitating a close symbiotic relationship. Moreover, each strain harbours the necessary genes for the assembly of a Type 9 Secretion System (T9SS) and the associated gliding motility apparatus. In addition to these common features, pathogenic strains AD1 and BL5, encode genes for the production of flexirubin type pigments and a number of unique non-ribosomal peptide synthesis (NRPS) gene clusters, suggesting a role for these uncharacterised traits in virulence. This study provides valuable insight into the potential ecological role of Aquimarina in the marine environment and the complex factors driving pathogenesis and symbiosis in this genus.
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Transcriptional response of Nautella italica R11 towards its macroalgal host uncovers new mechanisms of host-pathogen interaction.
Molecular Ecology, 2017Co-Authors: Jennifer Hudson, Melissa Gardiner, Nandan P. Deshpande, Suhelen EganAbstract:Macroalgae (seaweeds) are essential for the functioning of temperate marine ecosystems, but there is increasing evidence to suggest that their survival is under threat from anthropogenic stressors and disease. Nautella italica R11 is recognized as an aetiological agent of bleaching disease in the red alga, Delisea pulchra. Yet, there is a lack of knowledge surrounding the molecular mechanisms involved in this model host-pathogen interaction. Here we report that mutations in the gene encoding for a LuxR-type quorum sensing transcriptional regulator, RaiR, render N. italica R11 avirulent, suggesting this gene is important for regulating the expression of virulence phenotypes. Using an RNA sequencing approach, we observed a strong transcriptional response of N. italica R11 towards the presence of D. pulchra. In particular, genes involved in oxidative stress resistance, carbohydrate and central metabolism were upregulated in the presence of the host, suggesting a role for these functions in the opportunistic pathogenicity of N. italica R11. Furthermore, we show that RaiR regulates a subset of genes in N. italica R11, including those involved in metabolism and the expression of phage-related proteins. The outcome of this research reveals new functions important for virulence of N. italica R11 and contributes to our greater understanding of the complex factors mitigating microbial diseases in macroalgae.
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Exoproteome Analysis of the Seaweed Pathogen Nautella italica R11 Reveals Temperature-Dependent Regulation of RTX-Like Proteins.
Frontiers in Microbiology, 2017Co-Authors: Melissa Gardiner, Ling Zhong, Adam Bournazos, Claudia Maturana-martinez, Suhelen EganAbstract:Climate fluctuations have been linked to an increased prevalence of disease in seaweeds, including the red alga Delisea pulchra, which is susceptible to a bleaching disease caused by the bacterium Nautella italica R11 under elevated seawater temperatures. To further investigate the role of temperature in the induction of disease by N. italica R11, we assessed the effect of temperature on the expression of the extracellular proteome (exoproteome) in this bacterium. Label-free quantitative mass spectrometry was used to identify 207 proteins secreted into supernatant fraction, which is equivalent to 5% of the protein coding genes in the N. italica R11 genome. Comparative analysis demonstrated that expression of over 30% of the N. italica R11 exoproteome is affected by temperature. The temperature-dependent proteins include traits that could facilitate the ATP-dependent transport of amino acid and carbohydrate, as well as several uncharacterized proteins. Further, potential virulence determinants, including two RTX-like proteins, exhibited significantly higher expression in the exoproteome at the disease inducing temperature of 24°C relative to non-inducing temperature (16°C). This is the first study to demonstrate that temperature has an influence exoproteome expression in a macroalgal pathogen. The results have revealed several temperature regulated candidate virulence factors that may have a role in macroalgal colonization and invasion at elevated sea-surface temperatures, including novel RTX-like proteins.
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Microbial community function in the bleaching disease of the marine macroalgae Delisea pulchra.
Environmental Microbiology, 2017Co-Authors: Enrique Zozaya‐valdés, Suhelen Egan, Alexandra J. Roth‐schulze, Torsten ThomasAbstract:Summary Disease is increasingly viewed as a major factor impacting the health of both natural and cultured populations of marine organisms, including macroalgae. The red macroalga Delisea pulchra suffers from a bleaching disease resulting from host stress and infection by opportunistic bacterial pathogens. However, how pathogens cause the disease and how the entire macro algal-associated community is involved in the process is unclear. Here, we perform a metagenomic analysis of microbial communities associated with diseased and healthy D. pulchra across multiple bleaching events. Analysis of reconstructed 16S rRNA gene sequences showed that bacteria belonging to the families Rhodobacteraceae, Saprospiraceae and Flavobacteriaceae, including bacteria previously implicated in algal bleaching, to be enriched in diseased D. pulchra. Genes with predicted functions related to chemotaxis, motility, oxidative stress response, vitamin biosynthesis and nutrient acquisition were also prevalent in microbiomes of bleached algae, which may have a role in pathogenicity. Reconstruction of genomes that were abundant on bleached samples revealed that no single organism contains all bleaching-enriched functional genes. This observation indicates that potential virulence traits are distributed across multiple bacteria and that the disease in D. pulchra may result from a consortium of opportunistic pathogens, analogous to dysbiotic or polymicrobial diseases.
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Advance Access Publication Date: 26 February 2015 Short Communication
2016Co-Authors: Short Communication, Torsten Thomas, Melissa Gardiner, Suhelen EganAbstract:A glutathione peroxidase (GpoA) plays a role in the pathogenicity of Nautella italica strain R11 towards the red alga Delisea pulchr
R. De Nys - One of the best experts on this subject based on the ideXlab platform.
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Chemically mediated antifouling in the red alga Delisea pulchra
Marine Ecology Progress Series, 2006Co-Authors: Symon A. Dworjanyn, R. De Nys, Peter D. SteinbergAbstract:Using laboratory assays, we tested whether the secondary metabolites (furanones) on the surface of the red alga Delisea pulchra deter the settlement and growth of a range of ecologically relevant fouling organisms. D. pulchra and 4 other co-occurring seaweeds were almost exclusively fouled by other algae. Consequently, we carried out laboratory assays using propagules from 4 fouling algae (Ulva sp., Ceramium sp., Polysiphonia sp. and Ectocarpus siliculosis) representing the natural fouling community. The crude surface extract of D. pulchra at the same concentration as on the surface of the plant, the furanone fraction of this extract, and pure furnaones, deterred the settlement of fouling organisms in ecologically relevant assays. These data, coupled with knowledge of the surface concentration of furanones on D. pulchra and a mechanism by which furanones are sequestered onto the surface of the plant, provide a rigorous demonstration of chemically mediated antifouling.
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Inhibition of Luminescence and Virulence in the Black Tiger Prawn (Penaeus monodon) Pathogen Vibrio harveyi by Intercellular Signal Antagonists
Applied and Environmental Microbiology, 2000Co-Authors: Mike Manefield, R. De Nys, L Harris, Scott A Rice, Staffan KjellebergAbstract:Expression of luminescence in the Penaeus monodon pathogen Vibrio harveyi is regulated by an intercellular quorum sensing mechanism involving the synthesis and detection of two signaling molecules, one of which is N-hydroxy butanoyl-L-homoserine lactone and the other of which is uncharacterized. Indirect evidence has suggested that virulence, associated with a toxic extracellular protein, and luminescence in V. harveyi are coregulated. In this study the effects of an acylated homoserine lactone antagonist produced by the marine alga Delisea pulchra on luminescence and toxin production in a virulent strain of V. harveyi were analyzed. Luminescence and toxin production were both inhibited by the signal antagonist at concentrations that had no impact on growth. Toxin production was found to be prematurely induced in V. harveyi cultures incubated in a 10% conditioned medium. Additionally, a significant reduction in the toxicity of concentrated supernatant extracts from V. harveyi cultures incubated in the presence of the signal antagonist, as measured by in vivo toxicity assays in mice and prawns, was observed. These results suggest that intercellular signaling antagonists have potential utility in the control of V. harveyi prawn infections.
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Induction of metamorphosis in the sea urchin Holopneustes purpurascens by a metabolite complex from the algal host Delisea pulchra.
The Biological Bulletin, 2000Co-Authors: Jane E Williamson, Naresh Kumar, R. De Nys, David G. Carson, Peter D. SteinbergAbstract:Most benthic invertebrates have complex life cycles with planktonic larvae that return to the substratum to settle and metamorphose into a benthic stage. Although naturally produced chemical cues have long been thought to be important for the settlement or metamorphosis of invertebrate larvae, few ecologically relevant chemical cues have been clearly identified. The marine echinoid Holopneustes purpurascens has a complex life cycle, with a planktonic, nonfeeding dispersive larva that metamorphoses into a benthic stage that lives in the canopy of subtidal benthic algae such as the red alga Delisea pulchra and the kelp Ecklonia radiata. Recently recruited juveniles are found primarily on D. pulchra, and we hypothesized that this was in response to a chemical cue produced by this alga. Competent larvae metamorphosed in the presence of D. pulchra, or seawater surrounding this alga, but not in response to the presence of E. radiata or its extracts. A cue for metamorphosis was isolated and characterized from D....
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Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes
Marine Ecology Progress Series, 2000Co-Authors: Jeffrey T. Wright, R. De Nys, Peter D. SteinbergAbstract:We examine patterns of quantitative variation in halogenated furanones, secondary metabolites of Delisea pulchra (Rhodophyta; Bonnemaisoniales), and how this relates to variation in local abundance of herbivores and epiphytes. Fifteen populations of D. pulchra covering a distance of 650 km of temperate southeastern Australia were sampled. Concentrations of the 4 main furanones in D. pulchra (Compounds 1 to 4) showed large variability but there was no latitudinal trend to this variation. We found significant variation in the concentrations of both total and individual furanones among locations, between summer and winter, and between different life-history stages. Importantly, the range of total furanone concentration among plants within locations was large, often varying by an order of magnitude or more. A total of 5 species of herbivorous fish, 7 species of macroinvertebrate grazer and 6 groups of mesograzer (of varying taxonomic level) were found at the 15 locations. The abundance of both total macroinvertebrate grazers and total mesograzers known to consume D. pul- chra varied significantly among locations. However, correlations between furanones and the abun- dance of macroinvertebrate grazers and mesograzers at the scale of location were all weak and non- significant, as was the correlation between furanones and the abundance of epiphytes on D. pulchra. The large variability in concentrations of furanones, and the absence of any positive relationships between furanones, herbivores and epiphytes, suggest that quantitative variation in furanones in D. pulchra is not driven by population-level selection or induction, but is more likely to be a result of small-scale variation in environmental factors such as nutrients and light, and genetic differences among individual plants.
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Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra
Marine Biology, 1999Co-Authors: Symon A. Dworjanyn, R. De Nys, Peter D. SteinbergAbstract:The localisation of halogenated furanones, the biologically active secondary metabolites from the red alga Delisea pulchra (Greville), was determined by a combination of fluorescence microscopy, culture studies and quantitative chemical analyses. All types of evidence showed that furanones are localised in the central vesicle of gland cells in D. pulchra. These cells release furanones onto the surface of the plant, where they can be quantified using a newly developed surface extraction-technique. Levels of furanones on the surface of the plant were highest near the apical tips (≃100 ng cm−2), and decreased towards the base of the alga. Variation in furanone levels within the plant and variation in the number of gland cells followed a similar pattern. The localisation of furanones within gland cells in D. pulchra and the presence and concentrations of furanones on the surface of the plant are consistent with furanones functioning as antifoulants and in mediating other ecological interactions at the surface of the alga.
Mike Manefield - One of the best experts on this subject based on the ideXlab platform.
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Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover.
Microbiology, 2002Co-Authors: Mike Manefield, Peter D. Steinberg, Staffan Kjelleberg, Thomas Bovbjerg Rasmussen, Jens Bo Andersen, Morten Henzter, Michael GivskovAbstract:N-acyl-L-homoserine lactones (AHLs) are co-regulatory ligands required for control of the expression of genes encoding virulence traits in many Gram-negative bacterial species. Recent studies have indicated that AHLs modulate the cellular concentrations of LuxR-type regulatory proteins by binding and fortifying these proteins against proteolytic degradation (Zhu & Winans, 2001 R43 ). Halogenated furanones produced by the macroalga Delisea pulchra inhibit AHL-dependent gene expression. This study assayed for an in vivo interaction between a tritiated halogenated furanone and the LuxR protein of Vibrio fischeri overproduced in Escherichia coli. Whilst a stable interaction between the algal metabolite and the bacterial protein was not found, it was noted by Western analysis that the half-life of the protein is reduced up to 100-fold in the presence of halogenated furanones. This suggests that halogenated furanones modulate LuxR activity but act to destabilize, rather than protect, the AHL-dependent transcriptional activator. The furanone-dependent reduction in the cellular concentration of the LuxR protein was associated with a reduction in expression of a plasmid encoded P luxI –gfp(ASV) fusion suggesting that the reduction in LuxR concentration is the mechanism by which furanones control expression of AHL-dependent phenotypes. The mode of action by which halogenated furanones reduce cellular concentrations of the LuxR protein remains to be characterized.
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Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora
FEMS Microbiology Letters, 2001Co-Authors: Mike Manefield, Michael Givskov, Martin Welch, George P. C. Salmond, Staffan KjellebergAbstract:The plant pathogen Erwinia carotovora regulates expression of virulence factors and antibiotic production via an N-3-oxohexanoyl-L-homoserine lactone (3-oxo-C6-HSL) dependent quorum sensing mechanism. The marine alga Delisea pulchra produces halogenated furanones known to antagonise 3-oxo-C6-HSL activity. We have tested the effects of a halogenated furanone on the production of carbapenem, cellulase and protease in E. carotovora. Despite differences in the regulatory mechanisms controlling carbapenem and exoenzyme production each was inhibited by the algal metabolite. We present evidence to suggest that the furanone dependent inhibition of carbapenem production is a result of the disruption of the 3-oxo-C6-HSL dependent expression of the carABCDEFGH operon.
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inhibition of luminescence and virulence in the black tiger prawn penaeus monodon pathogen vibrio harveyi by intercellular signal antagonists
Applied and Environmental Microbiology, 2000Co-Authors: Mike Manefield, L Harris, Scott A Rice, Staffan KjellebergAbstract:Expression of luminescence in the Penaeus monodon pathogen Vibrio harveyi is regulated by an intercellular quorum sensing mechanism involving the synthesis and detection of two signaling molecules, one of which is N-hydroxy butanoyl-L-homoserine lactone and the other of which is uncharacterized. Indirect evidence has suggested that virulence, associated with a toxic extracellular protein, and luminescence in V. harveyi are coregulated. In this study the effects of an acylated homoserine lactone antagonist produced by the marine alga Delisea pulchra on luminescence and toxin production in a virulent strain of V. harveyi were analyzed. Luminescence and toxin production were both inhibited by the signal antagonist at concentrations that had no impact on growth. Toxin production was found to be prematurely induced in V. harveyi cultures incubated in a 10% conditioned medium. Additionally, a significant reduction in the toxicity of concentrated supernatant extracts from V. harveyi cultures incubated in the presence of the signal antagonist, as measured by in vivo toxicity assays in mice and prawns, was observed. These results suggest that intercellular signaling antagonists have potential utility in the control of V. harveyi prawn infections.
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Inhibition of Luminescence and Virulence in the Black Tiger Prawn (Penaeus monodon) Pathogen Vibrio harveyi by Intercellular Signal Antagonists
Applied and Environmental Microbiology, 2000Co-Authors: Mike Manefield, R. De Nys, L Harris, Scott A Rice, Staffan KjellebergAbstract:Expression of luminescence in the Penaeus monodon pathogen Vibrio harveyi is regulated by an intercellular quorum sensing mechanism involving the synthesis and detection of two signaling molecules, one of which is N-hydroxy butanoyl-L-homoserine lactone and the other of which is uncharacterized. Indirect evidence has suggested that virulence, associated with a toxic extracellular protein, and luminescence in V. harveyi are coregulated. In this study the effects of an acylated homoserine lactone antagonist produced by the marine alga Delisea pulchra on luminescence and toxin production in a virulent strain of V. harveyi were analyzed. Luminescence and toxin production were both inhibited by the signal antagonist at concentrations that had no impact on growth. Toxin production was found to be prematurely induced in V. harveyi cultures incubated in a 10% conditioned medium. Additionally, a significant reduction in the toxicity of concentrated supernatant extracts from V. harveyi cultures incubated in the presence of the signal antagonist, as measured by in vivo toxicity assays in mice and prawns, was observed. These results suggest that intercellular signaling antagonists have potential utility in the control of V. harveyi prawn infections.
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Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein.
Microbiology, 1999Co-Authors: Mike Manefield, Michael Givskov, Rocky De Nys, Steinberg Peter, Kumar Naresh, Read Roger, Staffan KjellebergAbstract:Acylated homoserine lactone (AHL)-mediated gene expression controls phenotypes involved in colonization, often specifically of higher organisms, in both marine and terrestrial environments. The marine red alga Delisea pulchra produces halogenated furanones which resemble AHLs structurally and show inhibitory activity at ecologically realistic concentrations in AHL bioassays. Evidence is presented that halogenated furanones displace tritiated OHHL [N-3-(oxohexanoyl)-L-homoserine lactone] from Escherichia coli cells overproducing LuxR with potencies corresponding to their respective inhibitory activities in an AHL-regulated bioluminescence assay, indicating that this is the mechanism by which furanones inhibit AHL-dependent phenotypes. Alternative mechanisms for this phenomenon are also addressed. General metabolic disruption was assessed with two-dimensional PAGE, revealing limited non-AHL-related effects. A direct chemical interaction between the algal compounds and AHLs, as monitored by 1H NMR spectroscopy, was shown not to occur in vitro. These results support the contention that furanones, at the concentrations produced by the alga, can control bacterial colonization of surfaces by specifically interfering with AHL-mediated gene expression at the level of the LuxR protein.