Synergistic Inhibition of the Lethal Fungal Pathogen Batrachochytrium dendrobatidis: The Combined Effect of Symbiotic Bacterial Metabolites and Antimicrobial Peptides of the Frog Rana muscosa

Myers, Jillian M.; Ramsey, Jeremy P.; Blackman, Alison L; Nichols, A. Elizabeth; Minbiole, Kevin P. C.; Harris, Reid N.

doi:10.1007/s10886-012-0170-2

Cited by 81 publications

(80 citation statements)

References 37 publications

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“…Third, the bacterial symbionts produce the antifungal compound only in association with the Hydra tissue, likely altering their metabolic state when changing their lifestyle from a free-living state to an epithelium colonizer. Fourth, antifungal compounds produced by the host and by the bacterial symbionts act together to inhibit fungal growth (Myers et al, 2012). Collectively, the observed differences between the in vitro and in vivo data suggest that simplified measures of in vitro microbial function may be insufficient or even misleading for evaluating the pathogen clearance potential of resident microbes.…”

Section: Discussionmentioning

confidence: 99%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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Epithelial surfaces of most animals are colonized by diverse microbial communities. Although it is generally agreed that commensal bacteria can serve beneficial functions, the processes involved are poorly understood. Here we report that in the basal metazoan Hydra, ectodermal epithelial cells are covered with a multilayered glycocalyx that provides a habitat for a distinctive microbial community. Removing this epithelial microbiota results in lethal infection by the filamentous fungus Fusarium sp. Restoring the complex microbiota in gnotobiotic polyps prevents pathogen infection. Although mono-associations with distinct members of the microbiota fail to provide full protection, additive and synergistic interactions of commensal bacteria are contributing to full fungal resistance. Our results highlight the importance of resident microbiota diversity as a protective factor against pathogen infections. Besides revealing insights into the in vivo function of commensal microbes in Hydra, our findings indicate that interactions among commensal bacteria are essential to inhibit pathogen infection.

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Section: Discussionmentioning

confidence: 99%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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“…As has been demonstrated for free-living bacteria (29), work with these symbiotic isolates can provide important information on bacterial function and can help to ground "-omics" data in organismal biology. In amphibians, there has been growing interest in the skin microbiota because some cutaneous bacterial symbionts can inhibit growth of the fungal pathogen Batrachochytrium dendrobatidis, which is responsible for global amphibian population declines and extinctions (25,(37)(38)(39)(40)(41)(42). Many initial studies of the amphibian skin microbiota focused on culturing bacteria to discover individual isolates with antifungal properties (culture-dependent approaches), while more recent studies have used next-generation sequencing to characterize the structural and functional diversity of these systems (culture-independent approaches).…”

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confidence: 99%

Most of the Dominant Members of Amphibian Skin Bacterial Communities Can Be Readily Cultured

Walke

Becker

Hughey

et al. 2015

Appl Environ Microbiol

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Currently, it is estimated that only 0.001% to 15% of bacteria in any given system can be cultured by use of commonly used techniques and media, yet culturing is critically important for investigations of bacterial function. Despite this situation, few studies have attempted to link culture-dependent and culture-independent data for a single system to better understand which members of the microbial community are readily cultured. In amphibians, some cutaneous bacterial symbionts can inhibit establishment and growth of the fungal pathogen Batrachochytrium dendrobatidis, and thus there is great interest in using these symbionts as probiotics for the conservation of amphibians threatened by B. dendrobatidis. The present study examined the portion of the culture-independent bacterial community (based on Illumina amplicon sequencing of the 16S rRNA gene) that was cultured with R2A low-nutrient agar and whether the cultured bacteria represented rare or dominant members of the community in the following four amphibian species: bullfrogs (Lithobates catesbeianus), eastern newts (Notophthalmus viridescens), spring peepers (Pseudacris crucifer), and American toads (Anaxyrus americanus). To determine which percentage of the community was cultured, we clustered Illumina sequences at 97% similarity, using the culture sequences as a reference database. For each amphibian species, we cultured, on average, 0.59% to 1.12% of each individual's bacterial community. However, the average percentage of bacteria that were culturable for each amphibian species was higher, with averages ranging from 2.81% to 7.47%. Furthermore, most of the dominant operational taxonomic units (OTUs), families, and phyla were represented in our cultures. These results open up new research avenues for understanding the functional roles of these dominant bacteria in host health. Microorganisms represent a large portion of global biodiversity and are responsible for many important ecological functions, yet the majority of microbes have not been cultured (1-3). It is estimated that only 0.001% to 15% of microbes can be cultured by use of commonly used techniques and media (2, 4), although some recent attempts at culturing the uncultured have been successful. For example, a prevalent and abundant human gut bacterium with potential biomedical importance was recently cultured by a gene-targeted approach (5). Still, only a third of known bacterial phyla have cultured representatives (6). Recent advances in culture-independent rRNA-based molecular approaches have allowed for a greater understanding of bacterial diversity (1,7,8), but in most cases, the only data we have about uncultured microbes are the DNA sequences obtained directly from the environment. Next-generation sequencing in some cases has led to the discovery of entire groups, such as the TM7 candidate division, often found in terrestrial, aquatic, and clinical habitats (9). This group is phylogenetically distinct and widespread yet has not been isolated in pure culture (9-12). There are also bacteri...

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“…It is possible that the effects of possible symbiotic bacteria in the animals may have reduced impact on immunity against the fungi in the new temperature regimes influenced by current climate (Daskin and Alford 2012). This view is credible in light of recent work (Myers et al 2012) that shows antimicrobial peptides (AMP) of the frog Rana muscosa secreted onto its skin may work synergistically with metabolites from endemic frog bacteria to confer resistance to the lethal chytridiomycosis. More specifically, Plethodon cinereus and skin bacterium Pseudomonas fluorescens may be a holobiont in that the bacterium limits the amount of AMP necessary from the frog.…”

Section: Anthropogenic Threats To Holobiont Global Ecologymentioning

confidence: 99%

Symbiosis—Evolution’s Co-Author

Zook

2015

Interdisciplinary Evolution Research

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Symbiotic integration is a primary contributor to the centerpiece of evolution, genetic novelty. Acquisition of foreign organisms or parts thereof, and potential subsequent assimilation and often internalization of one or several different genomes into another different entity are the foundational expressions upon which natural selection acts, particularly in eukaryotic organisms. Thus, the entire landscape of life-from cells to biomes-is substantially an evolving collection of chimeric communities. Competition may be pronounced and successful in evolution in large part because the competing organisms do not function as, and indeed are not, individuals. Moreover, growing evidence indicates symbiosis to be on a flexible continuum of physiological expression, often with real plasticity in the organisms' integrating life cycles. Therefore, so-called "mutualism", "parasitism", and "commensalism" as symbiotic reference points and analyses may be outdated and perhaps of dubious use. For example, fundamental ecological principles show us that "parasitism" among two different organisms is often of significant advantage to not only the "parasite" but its "host." Symbiosis system examples are here reviewed and redefined on a more meaningful evolutionary context; namely, symbiosis is the acquisition of one organism(s) by another different organism(s), and through subsequent long-term integration, new structures and metabolism emerge.

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Synergistic Inhibition of the Lethal Fungal Pathogen Batrachochytrium dendrobatidis: The Combined Effect of Symbiotic Bacterial Metabolites and Antimicrobial Peptides of the Frog Rana muscosa

Cited by 81 publications

References 37 publications

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Most of the Dominant Members of Amphibian Skin Bacterial Communities Can Be Readily Cultured

Symbiosis—Evolution’s Co-Author

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