ORCID Profile
0000-0003-4559-1046
Current Organisation
University of Massachusetts Boston
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Publisher: Public Library of Science (PLoS)
Date: 30-07-2014
Publisher: Wiley
Date: 10-06-2010
Publisher: Inter-Research Science Center
Date: 17-02-2012
DOI: 10.3354/DAO02429
Abstract: Amphibian conservation goals depend on effective disease-treatment protocols. Desirable protocols are species, life stage, and context specific, but currently few treatment options exist for hibians infected with the chytrid fungus Batrachochytrium dendrobatidis (Bd). Treatment options, at present, include antifungal drugs and heat therapy, but risks of toxicity and side-effects make these options untenable in some cases. Here, we report on the comparison of several novel treatments with a more generally accepted antifungal treatment in experimental scientific trials to treat Bd-infected frogs including Alytes obstetricans tadpoles and metamorphs, Bufo bufo and Limnodynastes peronii metamorphs, and Lithobates pipiens and Rana muscosa adults. The experimental treatments included commercial antifungal products (itraconazole, mandipropamid, steriplantN, and PIP Pond Plus), antimicrobial skin peptides from the Bd-resistant Pelophylax esculentus, microbial treatments (Pedobacter cryoconitis), and heat therapy (35°C for 24 h). None of the new experimental treatments were considered successful in terms of improving survival however, these results may advance future research by indicating the limits and potential of the various protocols. Caution in the use of itraconazole is warranted because of observed toxicity in metamorphic and adult frogs, even at low concentrations. Results suggest that rather than focusing on a single cure-all, erse lines of research may provide multiple options for treating Bd infection in hibians. Learning from 'failed treatments' is essential for the timely achievement of conservation goals and one of the primary aims for a publicly accessible treatment database under development.
Publisher: Elsevier BV
Date: 07-2015
Publisher: Wiley
Date: 06-2008
DOI: 10.1890/06-1842.1
Abstract: Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of hibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that hibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the hibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on hibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.
Publisher: Wiley
Date: 03-03-2013
DOI: 10.1111/ELE.12099
Abstract: Probiotic therapy through bioaugmentation is a feasible disease mitigation strategy based on growing evidence that microbes contribute to host defences of plants and animals. Amphibians are currently threatened by the rapid global spread of the pathogen, Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis. Bioaugmentation of locally occurring protective bacteria on hibians has mitigated this disease effectively in laboratory trials and one recent field trial. Areas still naïve to Bd provide an opportunity for conservationists to proactively implement probiotic strategies to prevent further hibian declines. In areas where Bd is endemic, bioaugmentation can facilitate repatriation of susceptible hibians currently maintained in assurance colonies. Here, we synthesise the current research in hibian microbial ecology and bioaugmentation to identify characteristics of effective probiotics in relation to their interactions with Bd, their host, other resident microbes and the environment. To target at-risk species and hibian communities, we develop s ling strategies and filtering protocols that result in probiotics that inhibit Bd under ecologically relevant conditions and persist on susceptible hibians. This filtering tool can be used proactively to guide hibian disease mitigation and can be extended to other taxa threatened by emerging infectious diseases.
Publisher: Wiley
Date: 08-2013
DOI: 10.1111/MEC.12431
Abstract: Microbial ecology of animals is taking on significance in the modern dialogue for the biology of species. Similar to a nuclear genome, the entire bacterial assemblage maintains an ancestral signal of the host's evolution leading to cophylogeny between the host and the microbes they harbour (Brucker & Bordenstein 2012b). The stability of such associations is of great interest as they provide a means for species to acquire new traits and genetic ersity that their own genomes lack (McFall-Ngai et al. 2013). The role of gut microbiota, for ex le, in host health and nutrition is widely recognized and a shared characteristic among animals. The role of bacteria colonizing the outside surfaces of animals is less well understood, but rather than random colonization, these microbes on skin, cuticles, scales and feathers in many cases provide benefits to the host. The symbiosis of leaf-cutter ants, their fungus gardens and their microbiota is a fascinating and complex system. Whether culture-independent bacterial ersity on the cuticle of leaf-cutter ants is high or highly constrained by subcuticular gland secretions is one prominent question. In this issue of Molecular Ecology, Andersen et al. (2013) show that leaf-cutting ants, Acromyrmex echinatior, maintain a dominant and colony-specific bacterium called Pseudonocardia on their cuticles (the laterocervical plates in particular). This bacterium is involved in protecting the ants and their fungal gardens from disease. Other fungus-gardening attine species as well as soil and vegetation can harbour Pseudonocardia. However, it was previously unknown how stable the bacterial strain-ant colony association was through the lifetime of the colony.
Publisher: American Society for Microbiology
Date: 26-04-2022
DOI: 10.1128/AEM.01818-21
Abstract: How host mucosal defenses interact, and influence disease outcome is critical in understanding host defenses against pathogens. A more detailed understanding is needed of the interactions between the host and the functioning of its mucosal defenses in pathogen defense.
Publisher: Springer Science and Business Media LLC
Date: 03-02-2020
DOI: 10.1186/S13059-019-1908-8
Abstract: Host-associated microbiomes, the microorganisms occurring inside and on host surfaces, influence evolutionary, immunological, and ecological processes. Interactions between host and microbiome affect metabolism and contribute to host adaptation to changing environments. Meta-analyses of host-associated bacterial communities have the potential to elucidate global-scale patterns of microbial community structure and function. It is possible that host surface-associated (external) microbiomes respond more strongly to variations in environmental factors, whereas internal microbiomes are more tightly linked to host factors. Here, we use the dataset from the Earth Microbiome Project and accumulate data from 50 additional studies totaling 654 host species and over 15,000 s les to examine global-scale patterns of bacterial ersity and function. We analyze microbiomes from non-captive hosts s led from natural habitats and find patterns with bioclimate and geophysical factors, as well as land use, host phylogeny, and trophic level/diet. Specifically, external microbiomes are best explained by variations in mean daily temperature range and precipitation seasonality. In contrast, internal microbiomes are best explained by host factors such as phylogeny/immune complexity and trophic level/diet, plus climate. Internal microbiomes are predominantly associated with top-down effects, while climatic factors are stronger determinants of microbiomes on host external surfaces. Host immunity may act on microbiome ersity through top-down regulation analogous to predators in non-microbial ecosystems. Noting gaps in geographic and host s ling, this combined dataset represents a global baseline available for interrogation by future microbial ecology studies.
Publisher: Wiley
Date: 10-2005
Publisher: Canadian Science Publishing
Date: 2000
Publisher: Elsevier BV
Date: 12-2012
DOI: 10.1016/J.MEEGID.2012.07.024
Abstract: Heterogeneity in immune defense effectors can benefit hosts encountering a variety of parasites and pathogens. Antimicrobial peptides (AMPs) are a erse set of immune defense effectors in many hibians, and are secreted from dermal granular glands to protect the skin from infection. Over 50 different skin peptides have been reported from the European water frog hybridogenic complex (Pelophylax esculentus complex), consisting of the hybrid P. esculentus, and the parent species Pelophylax lessonae and Pelophylax ridibundus. In central Europe the hybrid is sympatric with only P. lessonae, while in other areas all three species can co-occur. Amphibian immune defenses are likely under selective pressure from emerging pathogens such as the chytrid fungus Batrachochytrium dendrobatidis (Bd). To assess if hybridization affects immune defenses against Bd, we compared skin peptides of the three species in terms of (i) quantity, (ii) activity against Bd, (iii) repertoire, and (iv) stability. Hybrids secreted AMPs at higher quantities and with greater fungicidal activity compared to cohabiting P. lessonae. Compared to P. ridibundus, AMPs from hybrids were of similar quantity but slightly greater antifungal activity. Mass spectrometric analyses (MALDI-TOF) revealed that of all three species P. esculentus has the greatest peptide ersity, a repertoire inclusive of peptides occurring in either one or the other parent species. Measurements of degradation dynamics indicate that peptides remain relatively stable on the skin of all species for over an hour after induction of skin gland secretions. Our data demonstrate that the hybrid has more effective peptide defenses against Bd and a richer peptide repertoire than either parent species. Hybrid advantage in environments hosting virulent pathogens may contribute to disassortative mating preferences, and we suggest that AMP ersity may be analogous to major histocompatibility complex (MHC) heterozygosity by benefiting hosts encountering multiple parasites.
Publisher: Springer Science and Business Media LLC
Date: 18-02-2019
DOI: 10.1038/S41559-019-0798-1
Abstract: Animal-associated microbiomes are integral to host health, yet key biotic and abiotic factors that shape host-associated microbial communities at the global scale remain poorly understood. We investigated global patterns in hibian skin bacterial communities, incorporating s les from 2,349 in iduals representing 205 hibian species across a broad biogeographic range. We analysed how biotic and abiotic factors correlate with skin microbial communities using multiple statistical approaches. Global hibian skin bacterial richness was consistently correlated with temperature-associated factors. We found more erse skin microbiomes in environments with colder winters and less stable thermal conditions compared with environments with warm winters and less annual temperature variation. We used bioinformatically predicted bacterial growth rates, dormancy genes and antibiotic synthesis genes, as well as inferred bacterial thermal growth optima to propose mechanistic hypotheses that may explain the observed patterns. We conclude that temporal and spatial characteristics of the host's macro-environment mediate microbial ersity.
Publisher: Elsevier BV
Date: 03-2016
DOI: 10.1016/J.TIM.2015.12.010
Abstract: The contribution of emerging hibian diseases to the sixth mass extinction is driving innovative wildlife management strategies, including the use of probiotics. Bioaugmentation of the skin mucosome, a dynamic environment including host and microbial components, may not provide a generalized solution. Multi-omics technologies and ecological context underlie effective implementation.
Publisher: Wiley
Date: 31-10-2013
DOI: 10.1111/MEC.12510
Abstract: Skin‐associated bacteria of hibians are increasingly recognized for their role in defence against pathogens, yet we have little understanding of their basic ecology. Here, we use high‐throughput 16 S r RNA gene sequencing to examine the host and environmental influences on the skin microbiota of the cohabiting hibian species A naxyrus boreas, P seudacris regilla, T aricha torosa and L ithobates catesbeianus from the C entral V alley in C alifornia. We also studied populations of R ana cascadae over a large geographic range in the K lamath M ountain range of N orthern C alifornia, and across developmental stages within a single site. Dominant bacterial phylotypes on hibian skin included taxa from B acteroidetes, G ammaproteobacteria, A lphaproteobacteria, F irmicutes, S phingobacteria and A ctinobacteria. Amphibian species identity was the strongest predictor of microbial community composition. Secondarily, within a given hibian species, wetland site explained significant variation. Amphibian‐associated microbiota differed systematically from microbial assemblages in their environments. Rana cascadae tadpoles have skin bacterial communities distinct from postmetamorphic conspecifics, indicating a strong developmental shift in the skin microbes following metamorphosis. Establishing patterns observed in the skin microbiota of wild hibians and environmental factors that underlie them is necessary to understand skin symbiont community assembly, and ultimately, the role skin microbiota play in the extended host phenotype including disease resistance.
Publisher: Wiley
Date: 04-01-2016
DOI: 10.1111/ACV.12249
Publisher: Springer Science and Business Media LLC
Date: 13-11-2015
Publisher: Elsevier BV
Date: 12-2008
DOI: 10.1016/J.PEPTIDES.2008.09.006
Abstract: A peptide with the ability to release insulin from the rat BRIN-BD11 clonal beta cell line was isolated from norepinephrine-stimulated skin secretions of the Lemur leaf frog Hylomantis lemur Boulenger,1882. Determination of the primary structure (FLSLIPHVISALSSL.NH(2)) demonstrated that the peptide belongs to the phylloseptin family whose members have previously been identified in other Phyllomedusinae species. A synthetic replicate of the peptide, termed phylloseptin-L2, produced a significant stimulation of insulin release (134% of basal rate, P<0.01) from BRIN-BD11 cells at a concentration of 30 nM, with a maximum response (301% of basal rate, P<0.001) at a concentration of 3 microM. Phylloseptin-L2 did not stimulate release of the cytosolic enzyme, lactate dehydrogenase at concentrations up to 3 microM, indicating that the integrity of the plasma membrane had been preserved. The stimulatory action was maintained in the absence of extracellular Ca(2+) and in the presence of verapamil (50 microM) and diazoxide (300 microM) suggesting that mechanism of action of the peptide did not primarily involve influx of Ca(2+) or closure of ATP-sensitive K(+) channels. Administration of phylloseptin-L2 (50 nmol/kgbody weight) into mice significantly (P<0.05) increased total release of insulin and improved glucose tolerance during the 60 min period following an intraperitoneal injection of glucose (18 mmol/kgbody weight). It is concluded that the peptide shows potential for development into a therapeutically valuable agent for the treatment of Type 2 diabetes.
Publisher: Springer Science and Business Media LLC
Date: 04-10-2006
DOI: 10.1007/S00442-005-0228-8
Abstract: Many species of hibians in the wet tropics of Australia have experienced population declines linked with the emergence of a skin-invasive chytrid fungus, Batrachochytrium dendrobatidis. An innate defense, antimicrobial peptides produced by granular glands in the skin, may protect some species from disease. Here we present evidence that supports this hypothesis. We tested ten synthesized peptides produced by Australian species, and natural peptide mixtures from five Queensland rainforest species. Natural mixtures and most peptides tested in isolation inhibited growth of B. dendrobatidis in vitro. The three most active peptides (caerin 1.9, maculatin 1.1, and caerin 1.1) were found in the secretions of non-declining species (Litoria chloris, L. caerulea, and L. genimaculata). Although the possession of a potent isolated antimicrobial peptide does not guarantee protection from infection, non-declining species (L. lesueuri and L. genimaculata) inhabiting the rainforest of Queensland possess mixtures of peptides that may be more protective than those of the species occurring in the same habitat that have recently experienced population declines associated with chytridiomycosis (L. nannotis, L. rheocola, and Nyctimystes dayi). This study demonstrates that in vitro effectiveness of skin peptides correlates with the degree of decline in the face of an emerging pathogen. Further research is needed to assess whether this non-specific immune defense may be useful in predicting disease susceptibility in other species.
Publisher: Wiley
Date: 09-01-2012
Publisher: Springer Science and Business Media LLC
Date: 2011
Publisher: Frontiers Media SA
Date: 16-03-2016
Publisher: Wiley
Date: 28-01-2020
DOI: 10.1111/ACV.12565
Publisher: American Association for the Advancement of Science (AAAS)
Date: 30-03-2018
Abstract: The fungal disease chytridiomycosis has wreaked havoc on hibians worldwide. The disease is caused by the organism Batrachochytrium dendrobatidis and was first identified in the late 1990s. Voyles et al. revisited protected areas in Panama where catastrophic hibian losses were recorded a decade ago (see the Perspective by Collins). Although disease theory predicts that epidemics should result in reduced pathogenicity, they found no evidence for such a reduction. Despite this, the hibian community is displaying signs of recovery—including some species presumed extinct after the outbreak. Increased host resistance may be responsible for this recovery. Science , this issue p. 1517 see also p. 1458
Publisher: Elsevier BV
Date: 2006
DOI: 10.1016/J.DCI.2005.10.005
Abstract: The mountain yellow-legged frog (Rana muscosa) inhabits high elevation lakes in California that are largely undisturbed by human activities. In spite of this habitation in remote sites, populations continue to decline. Although predation by non-native fish is one cause for declines, some isolated populations in fishless lakes are suffering new declines. One possible cause of the current wave of declines is the introduction of the pathogenic chytrid fungus (Batrachochytrium dendrobatidis) which invades the adult skin to cause chytridiomycosis. In many hibian species, the skin is protected by antimicrobial peptides secreted into the mucous. Here we show that R. muscosa produces three previously unknown antimicrobial peptides belonging to the ranatuerin-2 and temporin-1 families of antimicrobial peptides. These three peptides, along with bradykinin, are the most abundant peptides in the skin secretions detected by mass spectrometry. Natural mixtures of peptides and in idual purified peptides strongly inhibit chytrid growth. The concentration of total peptides recovered from the skin of frogs following a mild norepinephrine induction is sufficient to inhibit chytrid growth in vitro. A comparison of the species susceptibility to chytridiomycosis and the antichytrid activity of peptides between R. muscosa and R. pipiens suggest that although R. muscosa produces more total skin peptides, it appears to be more vulnerable to B. dendrobatidis in nature. Possible differences in the antimicrobial peptide repertoires and life history traits of the two species that may account for differences in susceptibility are discussed.
Publisher: Public Library of Science (PLoS)
Date: 18-02-2021
DOI: 10.1371/JOURNAL.PPAT.1009234
Abstract: Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans ( Bsal ), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N . viridescens , adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N . viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy.
Publisher: Oxford University Press (OUP)
Date: 06-2009
Publisher: American Society for Microbiology
Date: 10-2015
DOI: 10.1128/AEM.01826-15
Abstract: The mucosal surfaces of wild and farmed aquatic vertebrates face the threat of many aquatic pathogens, including fungi. These surfaces are colonized by erse symbiotic bacterial communities that may contribute to fight infection. Whereas the gut microbiome of teleosts has been extensively studied using pyrosequencing, this tool has rarely been employed to study the compositions of the bacterial communities present on other teleost mucosal surfaces. Here we provide a topographical map of the mucosal microbiome of an aquatic vertebrate, the rainbow trout ( Oncorhynchus mykiss ). Using 16S rRNA pyrosequencing, we revealed novel bacterial ersity at each of the five body sites s led and showed that body site is a strong predictor of community composition. The skin exhibited the highest ersity, followed by the olfactory organ, gills, and gut. Flectobacillus was highly represented within skin and gill communities. Principal coordinate analysis and plots revealed clustering of external sites apart from internal sites. A highly erse community was present within the epithelium, as demonstrated by confocal microscopy and pyrosequencing. Using in vitro assays, we demonstrated that two Arthrobacter sp. skin isolates, a Psychrobacter sp. strain, and a combined skin aerobic bacterial s le inhibit the growth of Saprolegnia australis and Mucor hiemalis , two important aquatic fungal pathogens. These results underscore the importance of symbiotic bacterial communities of fish and their potential role for the control of aquatic fungal diseases.
Publisher: Public Library of Science (PLoS)
Date: 30-04-2014
Publisher: Wiley
Date: 14-08-2007
Publisher: Inter-Research Science Center
Date: 2003
DOI: 10.3354/DAO055065
Abstract: The emerging infectious disease chytridiomycosis is thought to have contributed to many of the recent alarming declines in hibian populations. Mortalities associated with these declines have often occurred during cooler seasons and at high elevations, suggesting that environmental temperature may be an important factor in disease emergence. We found that thermal environment affects the progress of the disease, and that housing frogs Litoria chloris at an environmental temperature of 37 degrees C for less than 16 h can clear them of the chytrid pathogen Batrachochytrium dendrobatidis. Our experiment demonstrated that elevated body temperatures similar to those experienced in behavioral fever and during normal thermoregulation can clear frogs of chytrid infection therefore, variation in thermoregulatory opportunities and behaviors are likely to contribute to the differences in disease incidence observed among host species, populations, and regions. Although further refinement of the technique is needed to encompass various host species, appropriately applied thermal manipulations of hibians and their enclosures may prove to be a safe and effective way of eliminating the fungal pathogen from captive hibian populations and: preventing accidental spread of the pathogen when animals are translocated or released from captivity.
Publisher: Oxford University Press (OUP)
Date: 2005
DOI: 10.1093/ICB/45.1.137
Abstract: One of the most urgent problems in conservation biology today is the continuing loss of hibian populations on a global scale. Recent hibian population declines in Australia, Central America, the western United States, Europe, and Africa have been linked to a pathogenic chytrid fungus, Batrachochytrium dendrobatidis, which infects the skin. The skin of hibians is critical for fluid balance, respiration, and transport of essential ions and the immune defense of the skin must be integrated with these physiological responses. One of the natural defenses of the skin is production of antimicrobial peptides in granular glands. Discharge of the granular glands is initiated by stimulation of sympathetic nerves. To determine whether antimicrobial skin peptides play a role in protection from invasive pathogens, purified antimicrobial peptides and natural peptide mixtures recovered from the skin secretions of a number of species have been assayed for growth inhibition of the chytrid fungus. The general findings are that most species tested have one or more antimicrobial peptides with potent activity against the chytrid fungus, and natural mixtures of peptides are also effective inhibitors of chytrid growth. This supports the hypothesis that antimicrobial peptides produced in the skin are an important defense against skin pathogens and may affect survival of populations. We also report on initial studies of peptide depletion using norepinephrine and the kinetics of peptide recovery following induction. Approximately 80 nmoles/g of norepinephrine is required to deplete peptides, and peptide stores are not fully recovered at three weeks following this treatment. Because many species have defensive peptides and yet suffer chytrid-associated population declines, it is likely that other factors (temperature, conditions of hydration, "stress," or pesticides) may alter normal defenses and allow for uncontrolled infection.
Publisher: Springer Science and Business Media LLC
Date: 12-12-2013
Publisher: Wiley
Date: 17-03-2017
Abstract: Improving host health through microbial manipulation requires untangling factors that shape the microbiome. There is currently little understanding of how initial community structure may drive the microbiota trajectory across host development or influence bacterial therapy outcomes. Probiotic baths of surface symbionts, Pseudomonas fluorescens and Flavobacterium johnsoniae were administered to 240 tadpoles of the midwife toad, Alytes obstetricans in semi-natural outdoor mesocosms originating from geographically and genetically distinct populations in Switzerland. Host bacterial and fungal assemblages were compared in tadpoles from the pond of origin, across metamorphosis, and in toadlets via microbial fingerprinting. Bacterial and fungal community structures differed significantly among populations and a microbial population signature persisted from the tadpole stage, through metamorphosis, and following probiotic treatment. A minimal core surface microbiota is described by persistence through development and by shared membership across populations. The impact of F. johnsoniae on the tadpole surface microbiome was assessed with shotgun metagenomics. Bacterial therapy reduced abundance, ersity, and functional repertoire compared to untreated controls. A correlation between host skin peptides and microbiota suggests a mechanism of host-directed symbiosis throughout development. Early developmental stages are ideal targets for hibian bacterial therapy that can govern a microbiome trajectory at critical timepoints and may impact susceptibility to disease.
Publisher: Oxford University Press (OUP)
Date: 2016
Publisher: Inter-Research Science Center
Date: 21-03-2017
DOI: 10.3354/DAO03097
Abstract: The ribosomal gene complex is a multi-copy region that is widely used for phylogenetic analyses of organisms from all 3 domains of life. In fungi, the copy number of the internal transcribed spacer (ITS) is used to detect abundance of pathogens causing diseases such as chytridiomycosis in hibians and white nose syndrome in bats. Chytridiomycosis is caused by the fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), and is responsible for declines and extinctions of hibians worldwide. Over a decade ago, a qPCR assay was developed to determine Bd prevalence and pathogen load. Here, we demonstrate the effect that ITS copy number variation in Bd strains can have on the estimation of prevalence and pathogen load. We used data sets from different hibian species to simulate how ITS copy number affects prevalence and pathogen load. In addition, we tested 2 methods (gBlocks® synthetic standards and digital PCR) to determine ITS copy number in Bd strains. Our results show that assumptions about the ITS copy number can lead to under- or overestimation of Bd prevalence and pathogen load. The use of synthetic standards replicated previously published estimates of ITS copy number, whereas dPCR resulted in estimates that were consistently lower than previously published estimates. Standardizing methods will assist with comparison across studies and produce reliable estimates of prevalence and pathogen load in the wild, while using the same Bd strain for exposure experiments and zoospore standards in qPCR remains the best method for estimating parameters used in epidemiological studies.
Publisher: Public Library of Science (PLoS)
Date: 29-01-2014
Publisher: Elsevier BV
Date: 08-2023
Publisher: Springer Science and Business Media LLC
Date: 24-02-2016
Publisher: Springer Science and Business Media LLC
Date: 11-02-2015
DOI: 10.1007/S10393-015-1010-Y
Abstract: Amphibian populations are decreasing worldwide due to a variety of factors. In South America, the chytrid fungus Batrachochytrium dendrobatidis (Bd) is linked to many population declines. The pathogenic effect of Bd on hibians can be inhibited by specific bacteria present on host skin. This symbiotic association allows some hibians to resist the development of the disease chytridiomycosis. Here, we aimed (1) to determine for the first time if specific anti-Bd bacteria are present on hibians in the Andes of Ecuador, (2) to monitor anti-Bd bacteria across developmental stages in a focal hibian, the Andean marsupial tree frog, Gastrotheca riobambae, that deposits larvae in aquatic habitats, and (3) to compare the Bd presence associated with host assemblages including 10 species at sites ranging in biogeography from Amazonian rainforest (450 masl) to Andes montane rainforest (3200 masl). We s led and identified skin-associated bacteria of frogs in the field using swabs and a novel methodology of aerobic counting plates, and a combination of morphological, biochemical, and molecular identification techniques. The following anti-Bd bacteria were identified and found to be shared among several hosts at high-elevation sites where Bd was present at a prevalence of 32.5%: Janthinobacterium lividum, Pseudomonas fluorescens, and Serratia sp. Bd were detected in Gastrotheca spp. and not detected in the lowlands (sites below 1000 masl). In G. riobambae, recognized Bd-resistant bacteria start to be present at the metamorphic stage. Overall bacterial abundance was significantly higher post-metamorphosis and on species s led at lower elevations. Further metagenomic studies are needed to evaluate the roles of host identity, life-history stage, and biogeography of the microbiota and their function in disease resistance.
Publisher: Elsevier BV
Date: 06-2009
DOI: 10.1016/J.PEPTIDES.2009.03.004
Abstract: Two families of structurally related C-terminally alpha-amidated antimicrobial peptides have been identified in norepinephrine-stimulated skin secretions of the midwife toad Alytes obstetricans (Alytidae). The alyteserin-1 peptides (Gly-Leu-Lys-(Asp/Glu)-Ile-Phe-Lys-Ala-Gly-Leu-Gly-Ser-Leu-Val-Lys-(Gly/Asn)-Ile-Ala-Ala-His-Val-Ala-(Asn/Ser).NH(2)) show limited structural similarity to the ascaphins from the skins of frogs of the family Leiopelmatidae. Alyteserin-2a (Ile-Leu-Gly-Lys-Leu-Leu-Ser-Thr-Ala-Ala-Gly-Leu-Leu-Ser-Asn-Leu.NH(2)) and alyteserin-2b and -2c (Ile-Leu-Gly-Ala-Ile-Leu-Pro-Leu-Val-Ser-Gly-Leu-Leu-Ser-(Asn/Ser)-Lys-Leu x NH(2)) show limited sequence identity with bombinin H6, present in the skins of frogs of the family Bombinatoridae. The alyteserin-1 peptides show selective growth inhibitory activity against the Gram-negative bacteria Escherichia coli (MIC=25 microM) whereas alyteserin-2a is more potent against the Gram-positive bacteria Staphylococcus aureus (MIC=50 microM). The hemolytic activity against human erythrocytes of all peptides tested is relatively weak (LC(50)>100 microM). The data demonstrate that the frogs belonging to the family Alytidae are among those producing dermal antimicrobial peptides that may represent a component of the animal's system of innate immunity.
Publisher: Wiley
Date: 02-05-2011
Publisher: PeerJ
Date: 11-06-2017
DOI: 10.7287/PEERJ.PREPRINTS.3017V1
Abstract: Emerging infectious diseases caused by fungal taxa are increasing and are placing a substantial burden on economies and ecosystems worldwide. Of the emerging fungal diseases, chytridomycosis caused by the fungus Batrachochytrium dendrobatidis (hereafter Bd) is causing a global hibian extinction. The host frog does have come internal innate immunity, as well as additional resistance through cutaneous microbial communities, leading to the development of probiotic bacterial therapies with mixed results. Unknown is the role of fungi in the protection against Bd infection, and as such, we examined the overlapping roles of bacterial and fungal microbiota in pathogen defense with a combination of high-throughput sequencing and culturing of symbiotic fungi from poison arrow frogs ( Dendrobates sp.). Our analyses revealed that abundance of cutaneous fungi contributed more to pathogen defense (~45%), than bacteria (~10%) and these differed from environmental microbiota. Further, we demonstrated that a fungal probiotic therapy did not induce an endocrine-immune reaction in contrast to bacterial probiotics that stressed hibian hosts and suppressed antimicrobial peptide responses, limiting their long-term colonization potential. Our results suggest that probiotic strategies against hibian fungal pathogens should refocus on host-associated and environmental fungi such as Penicillium and member of the families Chaetomiaceae and Lasiosphaeriaceae.
Publisher: Public Library of Science (PLoS)
Date: 19-09-2023
Publisher: Elsevier BV
Date: 12-2012
DOI: 10.1016/J.FUNBIO.2012.10.005
Abstract: Many parasites and pathogens suppress host immunity to maintain infection or initiate disease. On the skin of many hibians, defensive peptides are active against the fungus Batrachochytrium dendrobatidis (Bd), the causative agent of the emerging infectious disease chytridiomycosis. We tested the hypothesis that infection with the fungus may be linked to lower levels of defensive peptides. We s led both ambient (or constitutive) skin peptides on the ventral surface immediately upon capture, and stored skin peptides induced from granular glands by norepinephrine administration of Australian green-eyed treefrogs, Litoria serrata. Upon capture, uninfected frogs expressed an array of antimicrobial peptides on their ventral surface, whereas infected frogs had reduced skin peptide expression. Expression of ambient skin peptides differed with infection status, and antimicrobial peptides maculatin 1.1 and 2.1 were on average three times lower on infected frogs. However, the repertoire of skin peptides stored in granular glands did not differ with infection status on average equal quantities were recovered from infected and from uninfected frogs. Our results could have at least two causes: (1) frogs with reduced peptide expression are more likely to become infected (2) Bd infection interferes with defence peptides by inhibiting release or causing selective degradation of peptides on the skin surface. Immune evasion therefore may contribute to the pathogenesis of chytridiomycosis and a mechanistic understanding of this fungal strategy may lead to improved methods of disease control.
Publisher: Public Library of Science (PLoS)
Date: 15-08-2013
Publisher: Elsevier BV
Date: 09-2007
Publisher: Springer Science and Business Media LLC
Date: 16-05-2019
DOI: 10.1007/S00248-019-01385-9
Abstract: Probiotics can ameliorate diseases of humans and wildlife, but the mechanisms remain unclear. Host responses to interventions that change their microbiota are largely uncharacterized. We applied a consortium of four natural antifungal bacteria to the skin of endangered Sierra Nevada yellow-legged frogs, Rana sierrae, before experimental exposure to the pathogenic fungus Batrachochytrium dendrobatidis (Bd). The probiotic microbes did not persist, nor did they protect hosts, and skin peptide s ling indicated immune modulation. We characterized a novel skin defense peptide brevinin-1Ma (FLPILAGLAANLVPKLICSITKKC) that was downregulated by the probiotic treatment. Brevinin-1Ma was tested against a range of hibian skin cultures and found to inhibit growth of fungal pathogens Bd and B. salamandrivorans, but enhanced the growth of probiotic bacteria including Janthinobacterium lividum, Chryseobacterium ureilyticum, Serratia grimesii, and Pseudomonas sp. While commonly thought of as antimicrobial peptides, here brevinin-1Ma showed promicrobial function, facilitating microbial growth. Thus, skin exposure to probiotic bacterial cultures induced a shift in skin defense peptide profiles that appeared to act as an immune response functioning to regulate the microbiome. In addition to direct microbial antagonism, probiotic-host interactions may be a critical mechanism affecting disease resistance.
Publisher: Springer Science and Business Media LLC
Date: 2012
Publisher: Oxford University Press (OUP)
Date: 03-08-2011
DOI: 10.1093/ICB/ICR095
Abstract: Eco-immunology is the field of study that attempts to understand the functions of the immune system in the context of the host's environment. Amphibians are currently suffering devastating declines and extinctions in nearly all parts of the world due to the emerging infectious disease chytridiomycosis caused by the chytrid fungus, Batrachochytrium dendrobatidis. Because chytridiomycosis is a skin infection and remains confined to the skin, immune defenses of the skin are critical for survival. Skin defenses include secreted antimicrobial peptides and immunoglobulins as well as antifungal metabolites produced by symbiotic skin bacteria. Low temperatures, toxic chemicals, and stress inhibit the immune system and may impair natural defenses against B. dendrobatidis. Tadpoles' mouth parts can be infected by B. dendrobatidis. Damage to the mouth parts can impair growth, and the affected tadpoles maintain the pathogen in the environment even when adults have dispersed. Newly metamorphosing frogs appear to be especially vulnerable to infection and to the lethal effects of this pathogen because the immune system undergoes a dramatic reorganization at metamorphosis, and postmetamorphic defenses are not yet mature. Here we review our current understanding of hibian immune defenses against B. dendrobatidis and the ability of the pathogen to resist those defenses. We also briefly review what is known about the impacts of temperature, environmental chemicals, and stress on the host-pathogen interactions and suggest future directions for research.
Publisher: Frontiers Media SA
Date: 04-04-2017
Publisher: Wiley
Date: 10-04-2017
DOI: 10.1002/FEE.1481
Publisher: The Royal Society
Date: 12-06-2023
Abstract: The immune equilibrium model suggests that exposure to microbes during early life primes immune responses for pathogen exposure later in life. While recent studies using a range of gnotobiotic (germ-free) model organisms offer support for this theory, we currently lack a tractable model system for investigating the influence of the microbiome on immune system development. Here, we used an hibian species ( Xenopus laevis ) to investigate the importance of the microbiome in larval development and susceptibility to infectious disease later in life. We found that experimental reductions of the microbiome during embryonic and larval stages effectively reduced microbial richness, ersity and altered community composition in tadpoles prior to metamorphosis. In addition, our antimicrobial treatments resulted in few negative effects on larval development, body condition, or survival to metamorphosis. However, contrary to our predictions, our antimicrobial treatments did not alter susceptibility to the lethal fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in the adult life stage. While our treatments to reduce the microbiome during early development did not play a critical role in determining susceptibility to disease caused by Bd in X. laevis , they nevertheless indicate that developing a gnotobiotic hibian model system may be highly useful for future immunological investigations. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.
Publisher: Springer Science and Business Media LLC
Date: 19-06-2017
DOI: 10.1007/S00248-017-0997-8
Abstract: Amphibian granular glands provide a wide range of compounds on the skin that defend against pathogens and predators. We identified three bufadienolides-the steroid-like compounds arenobufagin, gamabufotalin, and telocinobufagin-from the boreal toad, Anaxyrus boreas, through liquid chromatography mass spectrometry (LC/MS). Compounds were detected both after inducing skin gland secretions and in constitutive mucosal rinses from toads. We described the antimicrobial properties of each bufadienolide against Batrachochytrium dendrobatidis (Bd), an hibian fungal pathogen linked with boreal toad population declines. All three bufadienolides were found to inhibit Bd growth at similar levels. The maximum Bd inhibition produced by arenobufagin, gamabufotalin, and telocinobufagin were approximately 50%, in contrast to the complete Bd inhibition shown by antimicrobial skin peptides produced by some hibian species. In addition, skin mucus s les significantly reduced Bd viability, and bufadienolides were detected in 15 of 62 s les. Bufadienolides also appeared to enhance growth of the anti-Bd bacterium Janthinobacterium lividum, and thus may be involved in regulation of the skin microbiome. Here, we localized skin bacteria within the mucus layer and granular glands of toads with fluorescent in situ hybridization. Overall, our results suggest that bufadienolides can function in antifungal defense on hibian skin and their production is a potentially convergent trait similar to antimicrobial peptide defenses found on the skin of other species. Further studies investigating bufadienolide expression across toad populations, their regulation, and interactions with other components of the skin mucosome will contribute to understanding the complexities of hibian immune defense.
Publisher: Springer Science and Business Media LLC
Date: 07-01-2017
DOI: 10.1007/S00248-016-0916-4
Abstract: The symbiotic microbes that grow in and on many organisms can play important roles in protecting their hosts from pathogen infection. While species ersity has been shown to influence community function in many other natural systems, the question of how species ersity of host-associated symbiotic microbes contributes to pathogen resistance is just beginning to be explored. Understanding ersity effects on pathogen resistance could be particularly helpful in combating the fungal pathogen Batrachochytrium dendrobatidis (Bd) which has caused dramatic population declines in many hibian species and is a major concern for hibian conservation. Our study investigates the ability of host-associated bacteria to inhibit the proliferation of Bd when grown in experimentally assembled biofilm communities that differ in species number and composition. Six bacterial species isolated from the skin of Cascades frogs (Rana cascadae) were used to assemble bacterial biofilm communities containing 1, 2, 3, or all 6 bacterial species. Biofilm communities were grown with Bd for 7 days following inoculation. More speciose bacterial communities reduced Bd abundance more effectively. This relationship between bacterial species richness and Bd suppression appeared to be driven by dominance effects-the bacterial species that were most effective at inhibiting Bd dominated multi-species communities-and complementarity: multi-species communities inhibited Bd growth more than monocultures of constituent species. These results underscore the notion that pathogen resistance is an emergent property of microbial communities, a consideration that should be taken into account when designing probiotic treatments to reduce the impacts of infectious disease.
Publisher: The Royal Society
Date: 28-09-2016
Abstract: Host-associated microbiomes perform many beneficial functions including resisting pathogens and training the immune system. Here, we show that hibians developing in captivity lose substantial skin bacterial ersity, primarily due to reduced ongoing input from environmental sources. We combined studies of wild and captive hibians with a database of over 1 000 strains that allows us to examine antifungal function of the skin microbiome. We tracked skin bacterial communities of 62 endangered boreal toads, Anaxyrus boreas , across 18 time points, four probiotic treatments, and two exposures to the lethal fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in captivity, and compared these to 33 s les collected from wild populations at the same life stage. As the hibians in captivity lost the Bd -inhibitory bacteria through time, the proportion of in iduals exposed to Bd that became infected rose from 33% to 100% in subsequent exposures. Inoculations of the Bd -inhibitory probiotic Janthinobacterium lividum resulted in a 40% increase in survival during the second Bd challenge, indicating that the effect of microbiome depletion was reversible by restoring Bd -inhibitory bacteria. Taken together, this study highlights the functional role of ongoing environmental inputs of skin-associated bacteria in mitigating a devastating hibian pathogen, and that long-term captivity decreases this defensive function.
Publisher: Springer Science and Business Media LLC
Date: 13-09-2012
DOI: 10.1007/S00359-012-0750-1
Abstract: Chemical signaling is a vital mode of communication for most organisms, including larval hibians. However, few studies have determined the identity or source of chemical compounds signaling hibian defensive behaviors, in particular, whether alarm pheromones can be actively secreted from tadpoles signaling danger to conspecifics. Here we exposed tadpoles of the common toad Bufo bufo and common frog Rana temporaria to known cues signaling predation risk and to potential alarm pheromones. In both species, an immediate reduction in swimming activity extending over an hour was caused by chemical cues from the predator Aeshna cyanea (dragonfly larvae) that had been feeding on conspecific tadpoles. However, B. bufo tadpoles did not detectably alter their behavior upon exposure to potential alarm pheromones, neither to their own skin secretions, nor to the abundant predator-defense peptide bradykinin. Thus, chemicals signaling active predation had a stronger effect than general alarm secretions of other common toad tadpoles. This species may invest in a defensive strategy alternative to communication by alarm pheromones, given that Bufonidae are toxic to some predators and not known to produce defensive skin peptides. Comparative behavioral physiology of hibian alarm responses may elucidate functional trade-offs in pheromone production and the evolution of chemical communication.
Publisher: Wiley
Date: 24-10-2007
Publisher: Wiley
Date: 23-03-2015
DOI: 10.1111/MEC.13135
Abstract: The introduction of next-generation sequencing has allowed for greater understanding of community composition of symbiotic microbial communities. However, determining the function of in idual members of these microbial communities still largely relies on culture-based methods. Here, we present results on the phylogenetic distribution of a defensive functional trait of cultured symbiotic bacteria associated with hibians. Amphibians are host to a erse community of cutaneous bacteria and some of these bacteria protect their host from the lethal fungal pathogen Batrachochytrium dendrobatidis (Bd) by secreting antifungal metabolites. We cultured over 450 bacterial isolates from the skins of Panamanian hibian species and tested their interactions with Bd using an in vitro challenge assay. For a subset of isolates, we also completed coculture experiments and found that culturing isolates with Bd had no effect on inhibitory properties of the bacteria, but it significantly decreased metabolite secretion. In challenge assays, approximately 75% of the bacterial isolates inhibited Bd to some extent and these inhibitory isolates were widely distributed among all bacterial phyla. Although there was no clear phylogenetic signal of inhibition, three genera, Stenotrophomonas, Aeromonas and Pseudomonas, had a high proportion of inhibitory isolates (100%, 77% and 73%, respectively). Overall, our results demonstrate that antifungal properties are phylogenetically widespread in symbiotic microbial communities of Panamanian hibians and that some functional redundancy for fungal inhibition occurs in these communities. We hope that these findings contribute to the discovery and development of probiotics for hibians that can mitigate the threat of chytridiomycosis.
Publisher: Elsevier BV
Date: 09-2007
DOI: 10.1016/J.TOXICON.2007.04.017
Abstract: Two peptides with differential cytolytic activity against bacteria, a fungus pathogenic to hibians, and mammalian cells were isolated from norepinephrine-stimulated skin secretions of the Lemur leaf frog Hylomantis lemur Boulenger, 1882. Dermaseptin-L1 (GLWSKIKEAAKAAGKAALNAVTGLVNQGDQPS) was active against the Gram-negative bacterium Escherichia coli (MIC=8 microM) but inactive against the Gram-positive bacterium Staphylococcus aureus. This peptide inhibited growth of zoospores of the chytrid fungus Batrachochytrium dendrobatidis at concentrations above 25 microM but did not completely inhibit growth at 100 microM. Phylloseptin-L1 (LLGMIPLAISAISALSKL.NH2) was active against S. aureus (MIC=8 microM) but was inactive against E. coli. This peptide also inhibited growth of B. dendrobatidis zoospores at concentrations above 25 microM with complete inhibition at 100 microM. Dermaseptin-L1 showed selective cytolytic activity against HepG2 human hepatoma-derived cells (LC50=45 microM) compared with human erythrocytes (LC50=200 microM) whereas phylloseptin-L1 was approximately equipotent against both HepG2 cells (LC50=35 microM) and erythrocytes (LC50=40 microM).
Publisher: Elsevier BV
Date: 12-2009
Publisher: Springer Science and Business Media LLC
Date: 26-03-2009
Abstract: Emerging infectious diseases threaten human and wildlife populations. Altered ecological interactions between mutualistic microbes and hosts can result in disease, but an understanding of interactions between host, microbes and disease-causing organisms may lead to management strategies to affect disease outcomes. Many hibian species in relatively pristine habitats are experiencing dramatic population declines and extinctions due to the skin disease chytridiomycosis, which is caused by the chytrid fungus Batrachochytrium dendrobatidis. Using a randomized, replicated experiment, we show that adding an antifungal bacterial species, Janthinobacterium lividum, found on several species of hibians to the skins of the frog Rana muscosa prevented morbidity and mortality caused by the pathogen. The bacterial species produces the anti-chytrid metabolite violacein, which was found in much higher concentrations on frog skins in the treatments where J. lividum was added. Our results show that cutaneous microbes are a part of hibians' innate immune system, the microbial community structure on frog skins is a determinant of disease outcome and altering microbial interactions on frog skins can prevent a lethal disease outcome. A bioaugmentation strategy may be an effective management tool to control chytridiomycosis in hibian survival assurance colonies and in nature.
Publisher: Frontiers Media SA
Date: 02-02-2016
Publisher: American Society for Microbiology
Date: 09-2010
DOI: 10.1128/IAI.00402-10
Abstract: Batrachochytrium dendrobatidis is a chytrid fungus that causes the lethal skin disease chytridiomycosis in hibians. It is regarded as an emerging infectious disease affecting erse hibian populations in many parts of the world. Because there are few model hibian species for immunological studies, little is known about immune defenses against B. dendrobatidis . We show here that the South African clawed frog, Xenopus laevis , is a suitable model for investigating immunity to this pathogen. After an experimental exposure, a mild infection developed over 20 to 30 days and declined by 45 days postexposure. Either purified antimicrobial peptides or mixtures of peptides in the skin mucus inhibited B. dendrobatidis growth in vitro . Skin peptide secretion was maximally induced by injection of norepinephrine, and this treatment resulted in sustained skin peptide depletion and increased susceptibility to infection. Sublethal X-irradiation of frogs decreased leukocyte numbers in the spleen and resulted in greater susceptibility to infection. Immunization against B. dendrobatidis induced elevated pathogen-specific IgM and IgY serum antibodies. Mucus secretions from X. laevis previously exposed to B. dendrobatidis contained significant amounts of IgM, IgY, and IgX antibodies that bind to B. dendrobatidis . These data strongly suggest that both innate and adaptive immune defenses are involved in the resistance of X. laevis to lethal B. dendrobatidis infections.
Publisher: Springer Science and Business Media LLC
Date: 09-2008
DOI: 10.1007/S10393-008-0190-0
Abstract: Chytridiomycosis is a globally emerging disease of hibians and the leading cause of population declines and extirpations at species- erse montane sites in Central America. We continued long-term monitoring efforts for the presence of the fungal pathogen Batrachochytrium dendrobatidis (Bd) and for hibian populations at two sites in western Panama, and we began monitoring at three new sites to the east. Population declines associated with chytridiomycosis emergence were detected at Altos de C ana National Park. We also detected Bd in three species east of the Panama Canal at Soberanía National Park, and prevalence data suggests that Bd may be enzootic in the lowlands of the park. However, no infected frogs were found further east at Tortí (prevalence <7.5% with 95% confidence). Our results suggest that Panama's erse and not fully described hibian communities east of the canal are at risk. Precise predictions of future disease emergence events are not possible until factors underlying disease emergence, such as dispersal, are understood. However, if the fungal pathogen spreads in a pattern consistent with previous disease events in Panama, then detection of Bd at Tortí and other areas east of the Panama Canal is imminent. Therefore, development of new management strategies and increased precautions for tourism, recreation, and biology are urgently needed.
Location: United States of America
No related grants have been discovered for Douglas Woodhams.