Browsing by Author "Becker, C. Guilherme"

Now showing 1 - 11 of 11
  • Thumbnail Image
    Item
    Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense
    (Royal Society of London, 2019) Greenspan, Sasha E.; Lyra, Mariana L.; Migliorini, Gustavo H.; Kersch-Becker, Monica F.; Bletz, Molly C.; Lisboa, Cybele Sabino; Pontes, Mariana R.; Ribeiro, Luisa P.; Neely, Wesley J.; Rezende, Felipe; Romero, Gustavo Q.; Woodhams, Douglas C.; Haddad, Celio F. B.; Toledo, Luis Felipe; Becker, C. Guilherme; University of Alabama Tuscaloosa; Universidade Estadual Paulista; University of Massachusetts Boston; Universidade Estadual de Campinas
    The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.
  • Thumbnail Image
    Item
    Bullfrog farms release virulent zoospores of the frog-killing fungus into the natural environment
    (Nature Portfolio, 2019) Ribeiro, Luisa P.; Carvalho, Tamilie; Becker, C. Guilherme; Jenkinson, Thomas S.; Leite, Domingos da Silva; James, TimothyY; Greenspan, Sasha E.; Toledo, Luis Felipe; Universidade Estadual de Campinas; University of Alabama Tuscaloosa; University of Michigan
    Bullfrog farming and trade practices are well-established, globally distributed, and economically valuable, but pose risks for biodiversity conservation. Besides their negative impacts on native amphibian populations as an invasive species, bullfrogs play a key role in spreading the frog-killing fungus Batrachochytrium dendrobatidis (Bd) in the natural environment. Bullfrogs are tolerant to Bd, meaning that they can carry high infection loads without developing chytridiomycosis. To test the potential of bullfrog farms as reservoirs for diverse and virulent chytrid genotypes, we quantified Bd presence, prevalence and infection loads across approximately 1,500 farmed bullfrogs and in the water that is released from farms into the environment. We also described Bd genotypic diversity within frog farms by isolating Bd from dozens of infected tadpoles. We observed individuals infected with Bd in all sampled farms, with high prevalence (reaching 100%) and high infection loads (average 71,029 zoospore genomic equivalents). Average outflow water volume from farms was high (60,000 L/day), with Bd zoospore concentration reaching approximately 50 million zoospores/L. Because virulent pathogen strains are often selected when growing in tolerant hosts, we experimentally tested whether Bd genotypes isolated from bullfrogs are more virulent in native anuran hosts compared to genotypes isolated from native host species. We genotyped 36 Bd isolates from two genetic lineages and found that Bd genotypes cultured from bullfrogs showed similar virulence in native toads when compared to genotypes isolated from native hosts. Our results indicate that bullfrog farms can harbor high Bd genotypic diversity and virulence and may be contributing to the spread of virulent genotypes in the natural environment. We highlight the urgent need to implement Bd monitoring and mitigation strategies in bullfrog farms to aid in the conservation of native amphibians.
  • Thumbnail Image
    Item
    Host-associated microbiomes are predicted by immune system complexity and climate
    (BMC, 2020) Woodhams, Douglas C.; Bletz, Molly C.; Becker, C. Guilherme; Bender, Hayden A.; Buitrago-Rosas, Daniel; Diebboll, Hannah; Huynh, Roger; Kearns, Patrick J.; Kueneman, Jordan; Kurosawa, Emmi; LaBumbard, Brandon C.; Lyons, Casandra; McNally, Kerry; Schliep, Klaus; Shankar, Nachiket; Tokash-Peters, Amanda G.; Vences, Miguel; Whetstone, Ross; University of Massachusetts Boston; Smithsonian Institution; Smithsonian Tropical Research Institute; University of Alabama Tuscaloosa; University of Rwanda; Braunschweig University of Technology
    Background 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. Results 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 samples to examine global-scale patterns of bacterial diversity and function. We analyze microbiomes from non-captive hosts sampled 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. Conclusions 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 diversity through top-down regulation analogous to predators in non-microbial ecosystems. Noting gaps in geographic and host sampling, this combined dataset represents a global baseline available for interrogation by future microbial ecology studies.
  • Thumbnail Image
    Item
    Host-associated microbiomes are predicted by immune system complexity and climate (vol 21, 23, 2020)
    (BMC, 2020) Woodhams, Douglas C.; Bletz, Molly C.; Becker, C. Guilherme; Bender, Hayden A.; Buitrago-Rosas, Daniel; Diebboll, Hannah; Huynh, Roger; Kearns, Patrick J.; Kueneman, Jordan; Kurosawa, Emmi; LaBumbard, Brandon C.; Lyons, Casandra; McNally, Kerry; Schliep, Klaus; Shankar, Nachiket; Tokash-Peters, Amanda G.; Vences, Miguel; Whetstone, Ross; University of Massachusetts Boston; Smithsonian Institution; Smithsonian Tropical Research Institute; University of Alabama Tuscaloosa; University of Rwanda; Braunschweig University of Technology
  • Thumbnail Image
    Item
    Low -load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian
    (Royal Society of London, 2019) Becker, C. Guilherme; Bletz, Molly C.; Greenspan, Sasha E.; Rodriguez, David; Lambertini, Carolina; Jenkinson, Thomas S.; Guimaraes, Paulo R., Jr.; Assis, Ana Paula A.; Geffers, Robert; Jarek, Michael; Toledo, Luis Felipe; Vences, Miguel; Haddad, Celio F. B.; University of Alabama Tuscaloosa; University of Massachusetts Boston; Texas State University San Marcos; Universidade Estadual de Campinas; University of California Berkeley; Universidade de Sao Paulo; Helmholtz Association; Helmholtz-Center for Infection Research; Braunschweig University of Technology; Universidade Estadual Paulista
    Wildlife disease dynamics are strongly influenced by the structure of host communities and their symbiotic microbiota. Conspicuous amphibian declines associated with the waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd) have been observed in aquatic-breeding frogs globally. However, less attention has been given to cryptic terrestrial-breeding amphibians that have also been declining in tropical regions. By experimentally manipulating multiple tropical amphibian assemblages harbouring natural microbial communities, we tested whether Bd spillover from naturally infected aquatic-breeding frogs could lead to Bd amplification and mortality in our focal terrestrial-breeding host: the pumpkin toadlet Brachycephalus pitanga. We also tested whether the strength of spillover could vary depending on skin bacterial transmission within host assemblages. Terrestrial-breeding toadlets acquired lethal spillover infections from neighbouring aquatic hosts and experienced dramatic but generally non protective shifts in skin bacterial composition primarily attributable to their Bd infections. By contrast, aquatic-bleeding amphibians maintained mild Bd infections and higher survival, with shifts in bacterial microbiomes that were unrelated to Bd infections. Our results indicate that Bd spillover from even mildly infected aquatic-breeding hosts may lead to dysbiosis and mortality in terrestrial-breeding species, underscoring the need to further investigate recent population declines of terrestrial-breeding amphibians in the tropics.
  • Thumbnail Image
    Item
    Low microbiome diversity in threatened amphibians from two biodiversity hotspots
    (BMC, 2022) Greenspan, Sasha E.; Peloso, Pedro; Fuentes-Gonzalez, Jesualdo A.; Bletz, Molly; Lyra, Mariana L.; Machado, Ibere F.; Martins, Renato A.; Medina, Daniel; Moura-Campos, Diego; Neely, Wesley J.; Preuss, Jackson; Sturaro, Marcelo J.; Vaz, Renata, I; Navas, Carlos A.; Toledo, Luis Felipe; Tozetti, Alexandro M.; Vences, Miguel; Woodhams, Douglas C.; Haddad, Celio F. B.; Pienaar, Jason; Becker, C. Guilherme; University of Alabama Tuscaloosa; Museu Paraense Emilio Goeldi; Universidade Federal do Para; Florida International University; University of Massachusetts Boston; Universidade Estadual Paulista; Universidade Federal de Sao Carlos; Secretaria Nacional de Ciencia, Tecnologia e Innovacin (SENACYT); Pennsylvania State University; Pennsylvania State University - University Park; Universidade Estadual de Campinas; Australian National University; Universidade do Oeste de Santa Catarina; Universidade Federal de Sao Paulo (UNIFESP); Universidade de Sao Paulo; Universidade do Vale do Rio dos Sinos (Unisinos); Braunschweig University of Technology
    Microbial diversity positively influences community resilience of the host microbiome. However, extinction risk factors such as habitat specialization, narrow environmental tolerances, and exposure to anthropogenic disturbance may homogenize host-associated microbial communities critical for stress responses including disease defense. In a dataset containing 43 threatened and 90 non-threatened amphibian species across two biodiversity hotspots (Brazil's Atlantic Forest and Madagascar), we found that threatened host species carried lower skin bacterial diversity, after accounting for key environmental and host factors. The consistency of our findings across continents suggests the broad scale at which low bacteriome diversity may compromise pathogen defenses in species already burdened with the threat of extinction.
  • Thumbnail Image
    Item
    Low resistance to chytridiomycosis in direct-developing amphibians
    (Nature Portfolio, 2017) Mesquita, Andrea F. C.; Lambertini, Carolina; Lyra, Mariana; Malagoli, Leo R.; James, Timothy Y.; Toledo, Luis Felipe; Haddad, Celio F. B.; Becker, C. Guilherme; Universidade Estadual Paulista; Universidade Estadual de Campinas; University of Michigan; University of Alabama Tuscaloosa
    Host-generalist pathogens sporadically infect naive hosts, potentially triggering epizootics. The waterborne fungus Batrachochytrium dendrobatidis (Bd) is linked to declines of hundreds of amphibian species with aquatic larvae. Although several population declines and extinctions attributed to Bd have been reported among cryptic species undergoing direct development away from water, epidemiological studies focused on these terrestrial frogs are lacking. Our field data support that terrestrial direct-developing hosts are less exposed to Bd during their ontogeny than species with aquatic larvae, and thus they might lack adaptive responses against waterborne chytrids. Using controlled laboratory experiments, we exposed wild-caught amphibian species with terrestrial and aquatic life histories to Bd and found that direct developers showed more rapid increases in infection loads and experienced higher mortality rates than species with aquatic larvae. Our findings provide novel information about host responses to generalist pathogens and specifically show that our focal direct developing species have low resistance to Bd infections. Finally, our results underscore that we should not ignore Bd as a potential threat to direct developing species simply because they are less exposed to Bd in nature; instead future amphibian conservation plans should include efforts to safeguard hundreds of direct-developing amphibian species globally.
  • Thumbnail Image
    Item
    Perspectives on invasive amphibians in Brazil
    (PLOS, 2017) Forti, Lucas Rodriguez; Becker, C. Guilherme; Tacioli, Leandro; Pereira, Vania Rosa; Santos, Andre Cid F. A.; Oliveira, Igor; Haddad, Celio F. B.; Toledo, Luis Felipe; Universidade Estadual de Campinas; Universidade de Sao Paulo; University of Alabama Tuscaloosa; Pontificia Universidade Catolica de Sao Paulo; Universidade Estadual Paulista
    Introduced species have the potential to become invasive and jeopardize entire ecosystems. The success of species establishing viable populations outside their original extent depends primarily on favorable climatic conditions in the invasive ranges. Species distribution modeling (SDM) can thus be used to estimate potential habitat suitability for populations of invasive species. Here we review the status of six amphibian species with invasive populations in Brazil (four domestic species and two imported species). We (i) modeled the current habitat suitability and future potential distribution of these six focal species, (ii) reported on the disease status of Eleutherodactylus johnstonei and Phyllodytes luteolus, and (iii) quantified the acoustic overlap of P. luteolus and Leptodactylus labyrinthicus with three cooccurring native species. Our models indicated that all six invasive species could potentially expand their ranges in Brazil within the next few decades. In addition, our SDMs predicted important expansions in available habitat for 2 out of 6 invasive species under future (2100) climatic conditions. We detected high acoustic niche overlap between invasive and native amphibian species, underscoring that acoustic interference might reduce mating success in local frogs. Despite the American bullfrog Lithobates catesbeianus being recognized as a potential reservoir for the frog-killing fungus Batrachochytrium dendrobatidis (Bd) in Brazil, we did not detect Bd in the recently introduced population of E. johnstonei and P. luteolus in the State of Sao Paulo. We emphasize that the number of invasive amphibian species in Brazil is increasing exponentially, highlighting the urgent need to monitor and control these populations and decrease potential impacts on the locally biodiverse wildlife.
  • Thumbnail Image
    Item
    Signatures of functional bacteriome structure in a tropical direct-developing amphibian species
    (BMC, 2022) Martins, Renato A.; Greenspan, Sasha E.; Medina, Daniel; Buttimer, Shannon; Marshall, Vanessa M.; Neely, Wesley J.; Siomko, Samantha; Lyra, Mariana L.; Haddad, Celio F. B.; Sao-Pedro, Vinicius; Becker, C. Guilherme; Universidade Federal de Sao Carlos; University of Alabama Tuscaloosa; Secretaria Nacional de Ciencia, Tecnologia e Innovacin (SENACYT); Pennsylvania State University; Pennsylvania State University - University Park; Universidade Estadual Paulista
    Background Host microbiomes may differ under the same environmental conditions and these differences may influence susceptibility to infection. Amphibians are ideal for comparing microbiomes in the context of disease defense because hundreds of species face infection with the skin-invading microbe Batrachochytrium dendrobatidis (Bd), and species richness of host communities, including their skin bacteria (bacteriome), may be exceptionally high. We conducted a landscape-scale Bd survey of six co-occurring amphibian species in Brazil's Atlantic Forest. To test the bacteriome as a driver of differential Bd prevalence, we compared bacteriome composition and co-occurrence network structure among the six focal host species. Results Intensive sampling yielded divergent Bd prevalence in two ecologically similar terrestrial-breeding species, a group with historically low Bd resistance. Specifically, we detected the highest Bd prevalence in Ischnocnema henselii but no Bd detections in Haddadus binotatus. Haddadus binotatus carried the highest bacteriome alpha and common core diversity, and a modular network partitioned by negative co-occurrences, characteristics associated with community stability and competitive interactions that could inhibit Bd colonization. Conclusions Our findings suggest that community structure of the bacteriome might drive Bd resistance in H. binotatus, which could guide microbiome manipulation as a conservation strategy to protect diverse radiations of direct-developing species from Bd-induced population collapses.
  • Thumbnail Image
    Item
    Skin microbiome correlates with bioclimate and Batrachochytrium dendrobatidis infection intensity in Brazil's Atlantic Forest treefrogs
    (Nature Portfolio, 2020) Ruthsatz, Katharina; Lyra, Mariana L.; Lambertini, Carolina; Belasen, Anat M.; Jenkinson, Thomas S.; Leite, Domingos da Silva; Becker, C. Guilherme; Haddad, Celio F. B.; James, Timothy Y.; Zamudio, Kelly R.; Toledo, Luis Felipe; Vences, Miguel; University of Hamburg; Universidade Estadual Paulista; Universidade de Sao Paulo; Universidade Estadual de Campinas; Cornell University; University of California Davis; University of Alabama Tuscaloosa; University of Michigan; Braunschweig University of Technology
    In Brazil's Atlantic Forest (AF) biodiversity conservation is of key importance since the fungal pathogen Batrachochytrium dendrobatidis (Bd) has led to the rapid loss of amphibian populations here and worldwide. The impact of Bd on amphibians is determined by the host's immune system, of which the skin microbiome is a critical component. The richness and diversity of such cutaneous bacterial communities are known to be shaped by abiotic factors which thus may indirectly modulate host susceptibility to Bd. This study aimed to contribute to understanding the environment-host-pathogen interaction determining skin bacterial communities in 819 treefrogs (Anura: Hylidae and Phyllomedusidae) from 71 species sampled across the AF. We investigated whether abiotic factors influence the bacterial community richness and structure on the amphibian skin. We further tested for an association between skin bacterial community structure and Bd co-occurrence. Our data revealed that temperature, precipitation, and elevation consistently correlate with richness and diversity of the skin microbiome and also predict Bd infection status. Surprisingly, our data suggest a weak but significant positive correlation of Bd infection intensity and bacterial richness. We highlight the prospect of future experimental studies on the impact of changing environmental conditions associated with global change on environment-host-pathogen interactions in the AF.
  • Thumbnail Image
    Item
    Spatiotemporal adaptive evolution of an MHC immune gene in a frog-fungus disease system
    (Springer Nature, 2021) Trujillo, Alexa L.; Hoffman, Eric A.; Becker, C. Guilherme; Savage, Anna E.; University of Central Florida; University of Alabama Tuscaloosa
    Genetic diversity of major histocompatibility complex (MHC) genes is linked to reduced pathogen susceptibility in amphibians, but few studies also examine broad spatial and temporal patterns of MHC and neutral genetic diversity. Here, we characterized range-wide MHC diversity in the Northern leopard frog, Rana pipiens, a species found throughout North America that is experiencing disease-related declines. We used previously sequenced neutral markers (mitochondrial DNA and microsatellites), sequenced an expressed MHC class IIss gene fragment, and measured infection prevalence and intensity of the global fungal pathogen Batrachochytrium dendrobatidis (Bd) across 14 populations. Four populations were sampled across two decades, enabling temporal comparisons of selection and demography. We recovered 37 unique MHC alleles, including 17 that were shared across populations. Phylogenetic and population genetic patterns between MHC and neutral markers were incongruent, and five MHC codon positions associated with peptide binding were under positive selection. MHC heterozygosity, but not neutral marker heterozygosity, was a significant factor explaining spatial patterns of Bd prevalence, whereas only environmental variables predicted Bd intensity. MHC allelic richness (AR) decreased significantly over time but microsatellite-based AR did not, highlighting a loss of functional immunogenetic diversity that may be associated with Bd selective pressures. MHC supertype 4 was significantly associated with an elevated risk of Bd infection, whereas one supertype 2 allele was associated with a nearly significant reduced risk of Bd. Taken together, these results provide evidence that positive selection contributes to MHC class IIss evolution in R. pipiens and suggest that functional MHC differences across populations may contribute to disease adaptation.