Soil bioaugmentation with amphibian cutaneous bacteria protects amphibian hosts from infection by Batrachochytrium dendrobatidis

Muletz, Carly R.; Myers, Jillian M.; Domangue, Rickie J.; Herrick, James B.; Harris, Reid N.

doi:10.1016/j.biocon.2012.03.022

Cited by 101 publications

(120 citation statements)

References 54 publications

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“…dendrobatidis bacteria (58), and augmenting these bacterial populations on susceptible amphibians during B. dendrobatidis epidemics may prove helpful. We expected J. lividum to be common because it was previously detected, using molecular approaches, on most individuals in two of three P. cinereus populations in Virginia (27,42,59). However, using culture methods, we found anti-B.…”

Section: Discussionmentioning

confidence: 78%

“…An active line of research has been to identify bacteria that inhibit B. dendrobatidis growth, here referred to as anti-B. dendrobatidis bacteria, and to use their geographic distribution to predict fungal disease outcome in the field (11,22,23) or to use them in trials of efficiency of bioaugmentation to mitigate B. dendrobatidis-associated disease symptoms (24)(25)(26)(27). To date, roughly 255 anti-B.…”

mentioning

confidence: 99%

“…For instance, three studies found no effect of an anti-B. dendrobatidis bacterial species, Janthinobacterium lividum, in reducing B. dendrobatidis-associated disease symptoms (29,31,32), even though J. lividum had previously been shown to be effective against B. dendrobatidis (25)(26)(27). This suggests that a bacterial species may not mitigate the impact of B. dendrobatidis on host health for all host species or in all environments.…”

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confidence: 99%

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Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

Muletz‐Wolz

DiRenzo

Yarwood³

et al. 2017

Appl Environ Microbiol

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Diverse bacteria inhabit amphibian skin; some of those bacteria inhibit growth of the fungal pathogen Batrachochytrium dendrobatidis. Yet there has been no systematic survey of anti-B. dendrobatidis bacteria across localities, species, and elevations. This is important given geographic and taxonomic variations in amphibian susceptibility to B. dendrobatidis. Our collection sites were at locations within the Appalachian Mountains where previous sampling had indicated low B. dendrobatidis prevalence. We determined the numbers and identities of anti-B. dendrobatidis bacteria on 61 Plethodon salamanders (37 P. cinereus, 15 P. glutinosus, 9 P. cylindraceus) via culturing methods and 16S rRNA gene sequencing. We sampled co-occurring species at three localities and sampled P. cinereus along an elevational gradient (700 to 1,000 meters above sea level [masl]) at one locality. We identified 50 anti-B. dendrobatidis bacterial operational taxonomic units (OTUs) and found that the degree of B. dendrobatidis inhibition was not correlated with relatedness. Five anti-B. dendrobatidis bacterial strains occurred on multiple amphibian species at multiple localities, but none were shared among all species and localities. The prevalence of anti-B. dendrobatidis bacteria was higher at Shenandoah National Park (NP), VA, with 96% (25/26) of salamanders hosting at least one anti-B. dendrobatidis bacterial species compared to 50% (7/14) at Catoctin Mountain Park (MP), MD, and 38% (8/21) at Mt. Rogers National Recreation Area (NRA), VA. At the individual level, salamanders at Shenandoah NP had more anti-B. dendrobatidis bacteria per individual ( ϭ 3.3) than those at Catoctin MP ( ϭ 0.8) and at Mt. Rogers NRA ( ϭ 0.4). All salamanders tested negative for B. dendrobatidis. Anti-B. dendrobatidis bacterial species are diverse in central Appalachian Plethodon salamanders, and their distribution varied geographically. The antifungal bacterial species that we identified may play a protective role for these salamanders.IMPORTANCE Amphibians harbor skin bacteria that can kill an amphibian fungal pathogen, Batrachochytrium dendrobatidis. Some amphibians die from B. dendrobatidis infection, whereas others do not. The bacteria that can kill B. dendrobatidis, called anti-B. dendrobatidis bacteria, are thought to influence the B. dendrobatidis infection outcome for the amphibian. Yet how anti-B. dendrobatidis bacterial species vary among amphibian species and populations is unknown. We determined the distribution of anti-B. dendrobatidis bacterial species among three salamander species (n ϭ 61) sampled at three localities. We identified 50 unique anti-B. dendrobatidis bacterial species and found that all of the tested salamanders were negative for B. dendrobatidis. Five anti-B. dendrobatidis bacterial species were commonly detected, suggesting a stable, functional association with these salamanders. The number of

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Section: Discussionmentioning

confidence: 78%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

Muletz‐Wolz

DiRenzo

Yarwood³

et al. 2017

Appl Environ Microbiol

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“…Furthermore, expression of phenotypic traits of a given species varies with ecological contexts, such as the single-strain vs. whole-community context, culture media vs. amphibian host, or laboratory vs. field. This diversity and context dependence may help explain why augmentation with Janthinobacterium isolates has been found to increase amphibian resistance to Bd infection in some contexts (42,57) but failed to protect amphibians in another study (65).…”

Section: Coordinated Laboratory and Field Studies Show Bd Infection Dmentioning

confidence: 99%

The pathogenBatrachochytrium dendrobatidisdisturbs the frog skin microbiome during a natural epidemic and experimental infection

Jani¹,

Briggs

2014

Proc. Natl. Acad. Sci. U.S.A.

227

294

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Significance Animals are inhabited by communities of microbes (the microbiome) that potentially interact with pathogens. Detailed studies of microbiome–pathogen interactions in nature are rare, and even when correlations are observed, determining causal relationships is challenging. The microbiome–pathogen relationship is of particular interest in the case of Batrachochytrium dendrobatidis , a chytrid fungus that infects the skin of amphibians and is causing amphibian declines worldwide. We documented a strong correlation between pathogen load and skin bacterial communities of frogs during natural disease episodes. We then showed experimentally that infection alters the microbiome, with similar bacteria responding in both laboratory and field. The results indicate that the chytrid pathogen drives changes in the amphibian skin microbiome during disease episodes in wild frogs.

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“…Several bacteria that reside on amphibian skin have been shown to inhibit the growth and survival of B. dendrobatidis in vitro. The presence of such bacteria on some host species or the application of such bacteria to some host species has proven to reduce the likelihood of infection and disease significantly (13)(14)(15)(16)(17). However, B. dendrobatidis is a rapidly evolving pathogen composed of multiple, deeply diverged lineages (18,19).…”

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confidence: 99%

Amphibian Symbiotic Bacteria Do Not Show a Universal Ability To Inhibit Growth of the Global Panzootic Lineage of Batrachochytrium dendrobatidis

Antwis

Preziosi

Harrison

et al. 2015

Appl Environ Microbiol

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cMicrobiomes associated with multicellular organisms influence the disease susceptibility of hosts. The potential exists for such bacteria to protect wildlife from infectious diseases, particularly in the case of the globally distributed and highly virulent fungal pathogen Batrachochytrium dendrobatidis of the global panzootic lineage (B. dendrobatidis GPL), responsible for mass extinctions and population declines of amphibians. B. dendrobatidis GPL exhibits wide genotypic and virulence variation, and the ability of candidate probiotics to restrict growth across B. dendrobatidis isolates has not previously been considered. Here we show that only a small proportion of candidate probiotics exhibited broad-spectrum inhibition across B. dendrobatidis GPL isolates. Moreover, some bacterial genera showed significantly greater inhibition than others, but overall, genus and species were not particularly reliable predictors of inhibitory capabilities. These findings indicate that bacterial consortia are likely to offer a more stable and effective approach to probiotics, particularly if related bacteria are selected from genera with greater antimicrobial capabilities. Together these results highlight a complex interaction between pathogens and host-associated symbiotic bacteria that will require consideration in the development of bacterial probiotics for wildlife conservation. Future efforts to construct protective microbiomes should incorporate bacteria that exhibit broad-spectrum inhibition of B. dendrobatidis GPL isolates.T he ability to withstand or mitigate pathogenic infection is partly determined by the host immune response. This has traditionally been examined in the context of immunity intrinsic to the host phenotype or genotype. However, all multicellular organisms coexist with a plethora of microbial organisms that are influential for host growth, development, and health (1). Although some of these microbes may be detrimental to the host, the importance of this microbiome in maintaining and improving host health is increasingly being recognized. The most obvious example of this is the gut community of humans: gut bacteria are essential for the digestion of food, but recent research has indicated that a healthy gut microbiome may also contribute to the prevention or moderation of liver, heart, and mental disease (reviewed in reference 2). The benefits to humans of a diverse microbiome are mirrored in other animal species, where the presence and composition of gut, buccal, and skin microbial communities have been linked to the occurrence and severity of both chronic and infectious disease (1).Conservation practitioners are increasingly interested in manipulating host microbiomes as a management tool to combat infectious diseases that pose threats and welfare issues to wild animals. The use of host-associated bacteria to act as probiotics for disease mitigation is already common practice in agriculture and human health (e.g., see the reviews in references 3 and 4). The fundamental strategy is to identify bacteria...

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Soil bioaugmentation with amphibian cutaneous bacteria protects amphibian hosts from infection by Batrachochytrium dendrobatidis

Cited by 101 publications

References 54 publications

Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

The pathogenBatrachochytrium dendrobatidisdisturbs the frog skin microbiome during a natural epidemic and experimental infection

Amphibian Symbiotic Bacteria Do Not Show a Universal Ability To Inhibit Growth of the Global Panzootic Lineage of Batrachochytrium dendrobatidis

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