RESUMO
Many studies have noted differences in microbes associated with animals reared in captivity compared to their wild counterparts, but few studies have examined how microbes change when animals are reintroduced to the wild after captive rearing. As captive assurance populations and reintroduction programs increase, a better understanding of how microbial symbionts respond during animal translocations is critical. We examined changes in microbes associated with boreal toads (Anaxyrus boreas), a threatened amphibian, after reintroduction to the wild following captive rearing. Previous studies demonstrate that developmental life stage is an important factor in amphibian microbiomes. We collected 16S marker-gene sequencing datasets to investigate: (i) comparisons of the skin, mouth, and fecal bacteria of boreal toads across four developmental life stages in captivity and the wild, (ii) tadpole skin bacteria before and after reintroduction to the wild, and (iii) adult skin bacteria during reintroduction to the wild. We demonstrated that differences occur across skin, fecal, and mouth bacterial communities in captive versus wild boreal toads, and that the degree of difference depends on developmental stage. Skin bacterial communities from captive tadpoles were more similar to their wild counterparts than captive post-metamorphic individuals were to their wild counterparts. When captive-reared tadpoles were introduced to a wild site, their skin bacteria changed rapidly to resemble wild tadpoles. Similarly, the skin bacterial communities of reintroduced adult boreal toads also shifted to resemble those of wild toads. Our results indicate that a clear microbial signature of captivity in amphibians does not persist after release into natural habitat.
Assuntos
Bufonidae , Microbiota , Humanos , Animais , Bufonidae/microbiologia , Larva/microbiologia , Bactérias/genética , Pele/microbiologiaRESUMO
Host-associated microbial biofilms can provide protection against pathogen establishment. In many host-microbe symbioses (including, but not limited to humans, plants, insects, and amphibians), there is a correlation between host-associated microbial diversity and pathogen infection risk. Diversity may prevent infection by pathogens through sampling effects and niche complementarity, but an alternative hypothesis may be that microbial biomass is confounded with diversity and that host-associated biofilms are deterring pathogen establishment through space preemption. In this study, we use the amphibian system as a model for host-microbe-pathogen interactions to ask two questions: (i) is bacterial richness confounded with biofilm thickness or cell density, and (ii) to what extent do biofilm thickness, cell density, and bacterial richness each deter the establishment of the amphibian fungal pathogen Batrachochytrium dendrobatidis? To answer these questions, we built a custom biofilm microcosm that mimics the host-environment interface by allowing nutrients to diffuse out of a fine-pore biofilm scaffolding. This created a competitive environment in which bacteria and the fungal pathogen compete for colonization space. We then challenged bacterial biofilms ranging in community richness, biofilm thickness, bacterial cell density, and B. dendrobatidis (also known as Bd)-inhibitory metabolite production with live B. dendrobatidis zoospores to determine how B. dendrobatidis establishment success on membranes varies. We found that biofilm thickness and B. dendrobatidis-inhibitory isolate richness work in complement to reduce B. dendrobatidis establishment success. This work underscores that physical aspects of biofilm communities can play a large role in pathogen inhibition, and in many studies, these traits are not studied. IMPORTANCE Our finding highlights the fact that diversity, as measured through 16S rRNA gene sequencing, may obscure the true mechanisms behind microbe-mediated pathogen defense and that physical space occupation by biofilm-forming symbionts may significantly contribute to pathogen protection. These findings have implications across a wide range of host-microbe systems since 16S rRNA gene sequencing is a standard tool used across many microbial systems. Further, our results are potentially relevant to many host-pathogen systems since host-associated bacterial biofilms are ubiquitous.
Assuntos
Quitridiomicetos , Microbiota , Anfíbios/genética , Anfíbios/microbiologia , Animais , Bactérias , Batrachochytrium , Biofilmes , Quitridiomicetos/genética , Humanos , Microbiota/genética , RNA Ribossômico 16S/genética , Pele/microbiologiaRESUMO
Pathogen success (risk and severity) is influenced by host-associated microbiota, but the degree to which variation in microbial community traits predict future infection presence/absence (risk) and load (severity) for the host is unknown. We conducted a time-series experiment by sampling the skin-associated bacterial communities of five amphibian species before and after exposure to the fungal pathogen, Batrachochytrium dendrobaditis (Bd). We sought to determine whether microbial community traits are predictors of, or are affected by, Bd infection risk and intensity. Our results show that richness of putative Bd-inhibitory bacteria strongly predicts infection risk, while the proportion of putative Bd-inhibitory bacteria predicts future infection intensity. Variation in microbial community composition is high across time and individual, and bacterial prevalence is low. Our findings demonstrate how ecological community traits of host-associated microbiota may be used to predict infection risk by pathogenic microbes.
Assuntos
Quitridiomicetos , Microbiota , Micoses , Anfíbios/microbiologia , Animais , Bactérias/genética , Batrachochytrium/genética , Micoses/epidemiologia , Micoses/microbiologia , Micoses/veterinária , Pele/microbiologiaRESUMO
Habitat conversion and fragmentation threaten biodiversity and disrupt species interactions. While parasites are recognized as ecologically important, the impacts of fragmentation on parasitism are poorly understood relative to other species interactions. This lack of understanding is in part due to confounding landscape factors that accompany fragmentation. Fragmentation experiments provide the opportunity to fill this knowledge gap by mechanistically testing how fragmentation affects parasitism while controlling landscape factors. In a large-scale, long-term experiment, we asked how fragmentation affects a host-parasite interaction between a skink and a parasitic nematode, which is trophically transmitted via a terrestrial amphipod intermediate host. We expected that previously observed amphipod declines resulting from fragmentation would result in decreased transmission of nematodes to skinks. In agreement, we found that nematodes were absent among skinks in the cleared matrix and that infections in fragments were about one quarter of those in continuous forest. Amphipods found in gut contents of skinks and collected from pitfall traps mirrored this pattern. A structural equation model supported the expectation that fragmentation disrupted this interaction by altering the abundance of amphipods and suggested that other variables are likely also important in mediating this effect. These findings advance understanding of how landscape change affects parasitism.
Assuntos
Lagartos , Infecções por Nematoides , Animais , Austrália , Biodiversidade , EcossistemaRESUMO
Amphibians undergo significant developmental changes during their life cycle, as they typically move from a primarily aquatic environment to a more terrestrial one. Amphibian skin is a mucosal tissue that assembles communities of symbiotic microbiota. However, it is currently not well understood as to where amphibians acquire their skin symbionts, and whether the sources of microbial symbionts change throughout development. In this study, we utilized data collected from four wild boreal toad populations (Anaxyrus boreas); specifically, we sampled the skin bacterial communities during toad development, including eggs, tadpoles, subadults and adults as well as environmental sources of bacteria (water, aquatic sediment and soil). Using 16S rRNA marker gene profiling coupled with SourceTracker, we show that while primary environmental sources remained constant throughout the life cycle, secondary sources of boreal toad symbionts significantly changed with development. We found that toad skin communities changed predictably across development and that two developmental disturbance events (egg hatching and metamorphosis) dictated major changes. Toad skin communities assembled to alternative stable states following each of these developmental disturbances. Using the predicted average rRNA operon copy number of the communities at each life stage, we showed how the skin bacterial communities undergo a successional pattern whereby "fast-growing" (copiotroph) generalist bacteria dominate first before "slow-growing" (oligotroph) specialized bacteria take over. Our study highlights how host-associated bacterial community assembly is tightly coupled to host development and that host-associated communities demonstrate successional patterns akin to those observed in free-living bacteria as well as macrofaunal communities.
Assuntos
Bufonidae/microbiologia , Interações entre Hospedeiro e Microrganismos/genética , Metamorfose Biológica/genética , Simbiose/genética , Animais , Bufonidae/genética , Bufonidae/crescimento & desenvolvimento , Larva/genética , Larva/crescimento & desenvolvimento , Larva/microbiologiaRESUMO
Host-associated microbiomes perform many beneficial functions including resisting pathogens and training the immune system. Here, we show that amphibians developing in captivity lose substantial skin bacterial diversity, primarily due to reduced ongoing input from environmental sources. We combined studies of wild and captive amphibians 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 samples collected from wild populations at the same life stage. As the amphibians in captivity lost the Bd-inhibitory bacteria through time, the proportion of individuals 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 amphibian pathogen, and that long-term captivity decreases this defensive function.
Assuntos
Bufonidae/microbiologia , Quitridiomicetos/patogenicidade , Micoses/veterinária , Probióticos , Animais , Microbiota , Micoses/prevenção & controleRESUMO
Despite growing evidence that parasites often alter nutrient flows through their hosts and can comprise a substantial amount of biomass in many systems, whether endemic parasites influence ecosystem nutrient cycling, and which nutrient pathways may be important, remains conjectural. A framework to evaluate how endemic parasites alter nutrient cycling across varied ecosystems requires an understanding of the following: (i) parasite effects on host nutrient excretion; (ii) ecosystem nutrient limitation; (iii) effects of parasite abundance, host density, host functional role and host excretion rate on nutrient flows; and (iv) how this infection-induced nutrient flux compares to other pools and fluxes. Pathogens that significantly increase the availability of a limiting nutrient within an ecosystem should produce a measurable ecosystem-scale response. Here, we combined field-derived estimates of trematode parasite infections in aquatic snails with measurements of snail excretion and tissue stoichiometry to show that parasites are capable of altering nutrient excretion in their intermediate host snails (dominant grazers). We integrated laboratory measurements of host nitrogen excretion with field-based estimates of infection in an ecosystem model and compared these fluxes to other pools and fluxes of nitrogen as measured in the field. Eighteen nitrogen-limited ponds were examined to determine whether infection had a measurable effect on ecosystem-scale nitrogen cycling. Because of their low nitrogen content and high demand for host carbon, parasites accelerated the rate at which infected hosts excreted nitrogen to the water column in a dose-response manner, thereby shifting nutrient stoichiometry and availability at the ecosystem scale. Infection-enhanced fluxes of dissolved inorganic nitrogen were similar to other commonly important environmental sources of bioavailable nitrogen to the system. Additional field measurements within nitrogen-limited ponds indicated that nitrogen flux rates from the periphyton to the water column in high-snail density/high-infection ponds were up to 50% higher than low-infection ponds. By altering host nutrient assimilation/excretion flexibility, parasites could play a widespread, but currently unrecognized, role in ecosystem nutrient cycling, especially when parasite and host abundances are high and hosts play a central role in ecosystem nutrient cycling.
Assuntos
Ecossistema , Ciclo do Nitrogênio , Caramujos/metabolismo , Caramujos/parasitologia , Trematódeos/metabolismo , Animais , Biomassa , Colorado , Lagoas , Infecções por Trematódeos/fisiopatologiaRESUMO
Animal-associated microbial communities can play major roles in the physiology, development, ecology, and evolution of their hosts, but the study of their diversity has yet focused on a limited number of host species. In this study, we used high-throughput sequencing of partial sequences of the bacterial 16S rRNA gene to assess the diversity of the gut-inhabiting bacterial communities of 212 specimens of tropical anuran amphibians from Brazil and Madagascar. The core gut-associated bacterial communities among tadpoles from two different continents strongly overlapped, with eight highly represented operational taxonomic units (OTUs) in common. In contrast, the core communities of adults and tadpoles from Brazil were less similar with only one shared OTU. This suggests a community turnover at metamorphosis. Bacterial diversity was higher in tadpoles compared to adults. Distinct differences in composition and diversity occurred among gut bacterial communities of conspecific tadpoles from different water bodies and after experimental fasting for 8 days, demonstrating the influence of both environmental factors and food on the community structure. Communities from syntopic tadpoles clustered by host species both in Madagascar and Brazil, and the Malagasy tadpoles also had species-specific isotope signatures. We recommend future studies to analyze the turnover of anuran gut bacterial communities at metamorphosis, compare the tadpole core communities with those of other aquatic organisms, and assess the possible function of the gut microbiota as a reservoir for protective bacteria on the amphibian skin.
Assuntos
Anuros/microbiologia , Fenômenos Fisiológicos Bacterianos , Trato Gastrointestinal/microbiologia , Animais , Bactérias/classificação , Bactérias/genética , Biodiversidade , Brasil , Larva , Madagáscar , Metamorfose Biológica , RNA Ribossômico 16S/genéticaRESUMO
Batrachochytrium dendrobatidis, a pathogenic chytrid fungus implicated in worldwide amphibian declines, is considered an amphibian specialist. Identification of nonamphibian hosts could help explain the virulence, heterogeneous distribution, variable rates of spread, and persistence of B. dendrobatidis in freshwater ecosystems even after amphibian extirpations. Here, we test whether mosquitofish (Gambusia holbrooki) and crayfish (Procambarus spp. and Orconectes virilis), which are syntopic with many amphibian species, are possible hosts for B. dendrobatidis. Field surveys in Louisiana and Colorado revealed that zoosporangia occur within crayfish gastrointestinal tracts, that B. dendrobatidis prevalence in crayfish was up to 29%, and that crayfish presence in Colorado wetlands was a positive predictor of B. dendrobatidis infections in cooccurring amphibians. In experiments, crayfish, but not mosquitofish, became infected with B. dendrobatidis, maintained the infection for at least 12 wk, and transmitted B. dendrobatidis to amphibians. Exposure to water that previously held B. dendrobatidis also caused significant crayfish mortality and gill recession. These results indicate that there are nonamphibian hosts for B. dendrobatidis and suggest that B. dendrobatidis releases a chemical that can cause host pathology, even in the absence of infection. Managing these biological reservoirs for B. dendrobatidis and identifying this chemical might provide new hope for imperiled amphibians.
Assuntos
Astacoidea/microbiologia , Quitridiomicetos/química , Ciprinodontiformes , Doenças dos Peixes/epidemiologia , Doenças dos Peixes/microbiologia , Micoses/veterinária , Animais , Quitridiomicetos/fisiologia , Colorado/epidemiologia , Doenças dos Peixes/transmissão , Conteúdo Gastrointestinal/microbiologia , Brânquias/microbiologia , Louisiana/epidemiologia , Micoses/epidemiologia , Micoses/transmissão , Prevalência , Modelos de Riscos Proporcionais , EsporângiosRESUMO
Skin-associated bacteria of amphibians are increasingly recognized for their role in defence against pathogens, yet we have little understanding of their basic ecology. Here, we use high-throughput 16S rRNA gene sequencing to examine the host and environmental influences on the skin microbiota of the cohabiting amphibian species Anaxyrus boreas, Pseudacris regilla, Taricha torosa and Lithobates catesbeianus from the Central Valley in California. We also studied populations of Rana cascadae over a large geographic range in the Klamath Mountain range of Northern California, and across developmental stages within a single site. Dominant bacterial phylotypes on amphibian skin included taxa from Bacteroidetes, Gammaproteobacteria, Alphaproteobacteria, Firmicutes, Sphingobacteria and Actinobacteria. Amphibian species identity was the strongest predictor of microbial community composition. Secondarily, within a given amphibian 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 amphibians 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.
Assuntos
Anfíbios/microbiologia , Bactérias/classificação , Microbiota , Ranidae/microbiologia , Pele/microbiologia , Animais , Bactérias/genética , Biodiversidade , California , DNA Bacteriano/genética , Lagos , Larva/microbiologia , RNA Ribossômico 16S/genética , Análise de Sequência de DNA , Microbiologia do Solo , Especificidade da Espécie , Microbiologia da ÁguaRESUMO
The amphibian fungal skin disease Batrachochytrium dendrobatidis (Bd) has caused major biodiversity losses globally. Several experimental trials have tested the use of Janthinobacterium lividum to reduce mortality due to Bd infections, usually in single-strain amendments. It is well-characterized in terms of its anti-Bd activity mechanisms. However, there are many other microbes that inhibit Bd in vitro, and not all experiments have demonstrated consistent results with J. lividum. We used a series of in vitro assays involving bacterial coculture with Bd lawns, bacterial growth tests in liquid broth, and Bd grown in bacterial cell-free supernatant (CFS) to determine: (i) which skin bacteria isolated from a locally endangered amphibian, namely, the Colorado boreal toad (Anaxyrus boreas boreas), are able to inhibit Bd growth; (ii) whether multistrain combinations are more effective than single-strains; and (iii) the mechanism behind microbe-microbe interactions. Our results indicate that there are some single strain and multistrain probiotics (especially including strains from Pseudomonas, Chryseobacterium, and Microbacterium) that are potentially more Bd-inhibitive than is J. lividum alone and that some combinations may lead to a loss of inhibition, potentially through antagonistic metabolite effects. Additionally, if J. lividum continues being developed as a wild boreal toad probiotic, we should investigate it in combination with Curvibacter CW54D, as they inhibited Bd additively and grew at a higher rate when combined than did either alone. This highlights the fact that combinations of probiotics function in variable and unpredictable ways as well as the importance of considering the potential for interactions among naturally resident host microbiota and probiotic additions. IMPORTANCE Batrachochytrium dendrobatidis (Bd) is a pathogen that infects amphibians globally and is causing a biodiversity crisis. Our research group studies one of the species affected by Bd, namely, the Colorado boreal toad (Anaxyrus boreas boreas). Many researchers focus their studies on one probiotic bacterial isolate called Janthinobacterium lividum, which slows Bd growth in lab cultures and is currently being field tested in Colorado boreal toads. Although promising, J. lividum is not consistently effective across all amphibian individuals or species. For Colorado boreal toads, we addressed whether there are other bacterial strains that also inhibit Bd (potentially better than does J. lividum) and whether we can create two-strain probiotics that function better than do single-strain probiotics. In addition, we evaluate which types of interactions occur between two-strain combinations and what these results mean in the context of adding a probiotic to an existing amphibian skin microbiome.
RESUMO
The amphibian skin pathogen Batrachochytrium dendrobatidis (Bd) has caused an ongoing biodiversity crisis, including in the locally endangered Colorado boreal toad (Anaxyrus boreas boreas). Although researchers have investigated the bacteria living on amphibian skin and how they interact with Bd, there is less information about fungal community members. This study describes (1) the diversity of culturable fungi from boreal toad skin, (2) which subset of these isolates is Bd-inhibitory, and (3) how Bd affects these isolates' growth and morphology. Most isolates were from the orders Capnodiales, Helotiales, and Pleosporales. Of 16 isolates tested for Bd-inhibition, two from the genus Neobulgaria and three from Pseudeurotium inhibited Bd. Fungal growth in co-culture with Bd varied with weak statistical support for Neobulgaria sp. (isolate BTF_36) and cf Psychrophila (isolate BTF_60) (p-values = 0.076 and 0.092, respectively). Fungal morphology remained unchanged in co-culture with Bd, however, these results could be attributed to low replication per isolate. Nonetheless, two fungal isolates' growth may have been affected by Bd, implying that fungal growth changes in Bd co-culture could be a variable worth measuring in the future (with higher replication). These findings add to the sparse but growing literature on amphibian-associated fungi and suggest further study may uncover the relevance of fungi to amphibian health and Bd infection.
RESUMO
Imagine a single pathogen that is responsible for mass mortality of over a third of an entire vertebrate class. For example, if a single pathogen were causing the death, decline and extinction of 30% of mammal species (including humans), the entire world would be paying attention. This is what has been happening to the world's amphibians - the frogs, toads and salamanders that are affected by the chytrid fungal pathogen, Batrachochytrium dendrobatidis (referred to as Bd), which are consequently declining at an alarming rate. It has aptly been described as the worst pathogen in history in terms of its effects on biodiversity (Kilpatrick et al. 2010). The pathogen was only formally described about 13 years ago (Longcore et al. 1999), and scientists are still in the process of determining where it came from and investigating the question: why now? Healthy debate has ensued as to whether Bd is a globally endemic organism that only recently started causing high mortality due to shifting host responses and/or environmental change (e.g. Pounds et al. 2006) or whether a virulent strain of the pathogen has rapidly disseminated around the world in recent decades, affecting new regions with a vengeance (e.g. Morehouse et al. 2003; Weldon et al. 2004; Lips et al. 2008). We are finally beginning to shed more light on this question, due to significant discoveries that have emerged as a result of intensive DNA-sequencing methods comparing Bd isolates from different amphibian species across the globe. Evidence is mounting that there is indeed a global panzootic lineage of Bd (BdGPL) in addition to what appear to be more localized endemic strains (Fisher et al. 2009; James et al. 2009; Farrer et al. 2011). Additionally, BdGPL appears to be a hypervirulent strain that has resulted from the hybridization of different Bd strains that came into contact in recent decades, and is now potentially replacing the less-virulent endemic strains of the pathogen (Farrer et al. 2011). In a new study published in this issue of Molecular Ecology, Schloegel et al. (2012) identify an additional unique Bd lineage that is endemic to the Atlantic Brazilian rainforests (Bd-Brazil) and provide striking evidence that the Bd-Brazil lineage has sexually recombined with the BdGPL lineage in an area where the two lineages likely came into contact as a result of classic anthropogenically mediated 'pathogen pollution'(see below). Fungal pathogens, including Bd, have the propensity to form recombinant lineages when allopatric populations that have not yet formed genetic reproductive barriers are provided with opportunities to intermingle, and virulent strains may be selected for because they tend to be highly transmissible (Fisher et al. 2012). As Schloegel et al. (2012) point out, the demonstrated ability for Bd to undergo meiosis may also mean that it has the capacity to form a resistant spore stage (as yet undiscovered), based on extrapolation from other sexually reproducing chytrids that all have spore stages.
Assuntos
Quimera/genética , Quitridiomicetos/genética , Genótipo , Rana catesbeiana/microbiologia , AnimaisRESUMO
Ecological theory predicts that species with restricted geographic ranges will have the highest probability of extinction, but species with extensive distributions and high population densities can also exhibit widespread population losses. In the western United States populations of northern leopard frogs (Lithobates pipiens)-historically one of the most widespread frogs in North America-have declined dramatically in abundance and geographic distribution. To assess the status of leopard frogs in Colorado and evaluate causes of decline, we coupled statewide surveys of 196 historically occupied sites with intensive sampling of 274 wetlands stratified by land use. We used an information-theoretic approach to evaluate the contributions of factors at multiple spatial extents in explaining the contemporary distribution of leopard frogs. Our results indicate leopard frogs have declined in Colorado, but this decline was regionally variable. The lowest proportion of occupied wetlands occurred in eastern Colorado (2-28%), coincident with urban development and colonization by non-native bullfrogs (Lithobates catesbeianus). Variables at several spatial extents explained observed leopard frog distributional patterns. In low-elevation wetlands introduced fishes, bullfrogs, and urbanization or suburbanization associated negatively with leopard frog occurrence, whereas wetland area was positively associated with occurrence. Leopard frogs were more abundant and widespread west of the Continental Divide, where urban development and bullfrog abundance were low. Although the pathogenic chytrid Batrachochytrium dendrobatidis (Bd) was not selected in our best-supported models, the nearly complete extirpation of leopard frogs from montane wetlands could reflect the individual or interactive effects of Bd and climate patterns. Our results highlight the importance of considering multiple, competing hypotheses to explain species declines, particularly when implicated factors operate at different spatial extents.
Assuntos
Conservação dos Recursos Naturais , Meio Ambiente , Espécies Introduzidas , Rana catesbeiana , Rana pipiens , Animais , Biodiversidade , Colorado , Espécies em Perigo de Extinção , Densidade Demográfica , Dinâmica Populacional , Rana catesbeiana/microbiologia , Rana pipiens/microbiologia , Reforma UrbanaRESUMO
Host-associated microbes can interact with macro-organisms in a number of ways that affect host health. Few studies of host-associated microbiomes, however, focus on fungi. In addition, it is difficult to discern whether a fungal organism found in or on an ectotherm host is associating with it in a durable, symbiotic interaction versus a transient one, and to what extent the habitat and host share microbes. We seek to identify these host-microbe interactions on an amphibian, the Colorado boreal toad (Anaxyrus boreas boreas). We sequenced the ITS1 region of the fungal community on the skin of wild toads (n = 124) from four sites in the Colorado Rocky Mountains, across its physiologically dynamic developmental life stages. We also sampled the common habitats used by boreal toads: water from their natal wetland and aquatic pond sediment. We then examined diversity patterns within different life stages, between host and habitat, and identified fungal taxa that could be putatively host-associated with toads by using an indicator species analysis on toad versus environmental samples. Host and habitat were strikingly similar, with the exception of toad eggs. Post-hatching toad life stages were distinct in their various fungal diversity measures. We identified eight fungal taxa that were significantly associated with eggs, but no other fungal taxa were associated with other toad life stages compared with their environmental habitat. This suggests that although pre- and post-metamorphic toad life stages differ from each other, the habitat and host fungal communities are so similar that identifying obligate host symbionts is difficult with the techniques used here. This approach does, however, leverage sequence data from host and habitat samples to predict which microbial taxa are host-associated versus transient microbes, thereby condensing a large set of sequence data into a smaller list of potential targets for further consideration.
Assuntos
Bufonidae/microbiologia , Quitridiomicetos/isolamento & purificação , Interações entre Hospedeiro e Microrganismos/genética , Simbiose/genética , Animais , Bufonidae/genética , Quitridiomicetos/genética , Colorado , Microbiota/genética , Pele/microbiologiaRESUMO
Worldwide increases in human and wildlife diseases have challenged ecologists to understand how large-scale environmental changes affect host-parasite interactions. One of the most profound changes to Earth's ecosystems is the alteration of global nutrient cycles, including those of phosphorus (P) and especially nitrogen (N). Along with the obvious direct benefits of nutrient application for food production, anthropogenic inputs of N and P can indirectly affect the abundance of infectious and noninfectious pathogens. The mechanisms underpinning observed correlations, however, and how such patterns vary with disease type, have long remained conjectural. Here, we highlight recent experimental advances to critically evaluate the relationship between environmental nutrient enrichment and disease. Given the interrelated nature of human and wildlife disease emergence, we include a broad range of human and wildlife examples from terrestrial, marine, and freshwater ecosystems. We examine the consequences of nutrient pollution on directly transmitted, vector-borne, complex life cycle, and noninfectious pathogens, including West Nile virus, malaria, harmful algal blooms, coral reef diseases, and amphibian malformations. Our synthetic examination suggests that the effects of environmental nutrient enrichment on disease are complex and multifaceted, varying with the type of pathogen, host species and condition, attributes of the ecosystem, and the degree of enrichment; some pathogens increase in abundance whereas others decline or disappear. Nevertheless, available evidence indicates that ecological changes associated with nutrient enrichment often exacerbate infection and disease caused by generalist parasites with direct or simple life cycles. Observed mechanisms include changes in host/vector density, host distribution, infection resistance, pathogen virulence or toxicity, and the direct supplementation of pathogens. Collectively, these pathogens may be particularly dangerous because they can continue to cause mortality even as their hosts decline, potentially leading to sustained epidemics or chronic pathology. We suggest that interactions between nutrient enrichment and disease will become increasingly important in tropical and subtropical regions, where forecasted increases in nutrient application will occur in an environment rich with infectious pathogens. We emphasize the importance of careful disease management in conjunction with continued intensification of global nutrient cycles.
Assuntos
Doenças Transmissíveis Emergentes/veterinária , Nitrogênio , Fósforo , Animais , Animais Selvagens , Doenças Transmissíveis Emergentes/transmissão , Ecossistema , Fertilizantes , Interações Hospedeiro-Patógeno , Humanos , Modelos Biológicos , ZoonosesRESUMO
Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from â¼900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Furthermore, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors convergently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome.IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes.
Assuntos
Evolução Biológica , Aves , Quirópteros , Microbioma Gastrointestinal , Vertebrados , Animais , Biologia Computacional/métodos , Metagenoma , Metagenômica/métodosRESUMO
Animal microbiomes play an important role in dietary adaptation, yet the extent to which microbiome changes exhibit parallel evolution is unclear. Of particular interest is an adaptation to extreme diets, such as blood, which poses special challenges in its content of proteins and lack of essential nutrients. In this study, we assessed taxonomic signatures (by 16S rRNA amplicon profiling) and potential functional signatures (inferred by Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt)) of haematophagy in birds and bats. Our goal was to test three alternative hypotheses: no convergence of microbiomes, convergence in taxonomy and convergence in function. We find a statistically significant effect of haematophagy in terms of microbial taxonomic convergence across the blood-feeding bats and birds, although this effect is small compared to the differences found between haematophagous and non-haematophagous species within the two host clades. We also find some evidence of convergence at the predicted functional level, although it is possible that the lack of metagenomic data and the poor representation of microbial lineages adapted to haematophagy in genome databases limit the power of this approach. The results provide a paradigm for exploring convergent microbiome evolution replicated with independent contrasts in different host lineages. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.
Assuntos
Bactérias/genética , Aves/genética , Quirópteros/genética , Microbioma Gastrointestinal , Animais , Bactérias/classificação , Bactérias/isolamento & purificação , Evolução Biológica , Aves/microbiologia , Aves/fisiologia , Quirópteros/microbiologia , Quirópteros/fisiologia , DNA Bacteriano/genética , Comportamento Alimentar , Filogenia , RNA Ribossômico 16S/genéticaRESUMO
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 amphibian skin bacterial communities, incorporating samples from 2,349 individuals representing 205 amphibian species across a broad biogeographic range. We analysed how biotic and abiotic factors correlate with skin microbial communities using multiple statistical approaches. Global amphibian skin bacterial richness was consistently correlated with temperature-associated factors. We found more diverse 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 diversity.