Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria

Symbiotic bacteria may dampen the impacts of infectious diseases on hosts by inhibiting pathogen growth. However, our understanding of the generality of pathogen inhibition by different bacterial taxa across pathogen genotypes and environmental conditions is limited. Bacterial inhibitory properties...

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Main Authors: Carly R. Muletz-Wolz, Jose G. Almario, Samuel E. Barnett, Graziella V. DiRenzo, An Martel, Frank Pasmans, Kelly R. Zamudio, Luís Felipe Toledo, Karen R. Lips
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01551/full
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author Carly R. Muletz-Wolz
Carly R. Muletz-Wolz
Jose G. Almario
Samuel E. Barnett
Samuel E. Barnett
Graziella V. DiRenzo
Graziella V. DiRenzo
An Martel
Frank Pasmans
Kelly R. Zamudio
Luís Felipe Toledo
Karen R. Lips
author_facet Carly R. Muletz-Wolz
Carly R. Muletz-Wolz
Jose G. Almario
Samuel E. Barnett
Samuel E. Barnett
Graziella V. DiRenzo
Graziella V. DiRenzo
An Martel
Frank Pasmans
Kelly R. Zamudio
Luís Felipe Toledo
Karen R. Lips
author_sort Carly R. Muletz-Wolz
collection DOAJ
description Symbiotic bacteria may dampen the impacts of infectious diseases on hosts by inhibiting pathogen growth. However, our understanding of the generality of pathogen inhibition by different bacterial taxa across pathogen genotypes and environmental conditions is limited. Bacterial inhibitory properties are of particular interest for the amphibian-killing fungal pathogens (Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans), for which probiotic applications as conservation strategies have been proposed. We quantified the inhibition strength of five putatively B. dendrobatidis-inhibitory bacteria isolated from woodland salamander skin against six Batrachochytrium genotypes at two temperatures (12 and 18°C). We selected six genotypes from across the Batrachochytrium phylogeny: B. salamandrivorans, B. dendrobatidis-Brazil and four genotypes of the B. dendrobatidis Global Panzootic Lineage (GPL1: JEL647, JEL404; GPL2: SRS810, JEL423). We performed 96-well plate challenge assays in a full factorial design. We detected a Batrachochytrium genotype by temperature interaction on bacterial inhibition score for all bacteria, indicating that bacteria vary in ability to inhibit Batrachochytrium depending on pathogen genotype and temperature. Acinetobacter rhizosphaerae moderately inhibited B. salamandrivorans at both temperatures (μ = 46–53%), but not any B. dendrobatidis genotypes. Chryseobacterium sp. inhibited three Batrachochytrium genotypes at both temperatures (μ = 5–71%). Pseudomonas sp. strain 1 inhibited all Batrachochytrium genotypes at 12°C and four Batrachochytrium genotypes at 18°C (μ = 5–100%). Pseudomonas sp. strain 2 and Stenotrophomonas sp. moderately to strongly inhibited all six Batrachochytrium genotypes at both temperatures (μ = 57–100%). All bacteria consistently inhibited B. salamandrivorans. Using cluster analysis of inhibition scores, we found that more closely related Batrachochytrium genotypes grouped together, suggesting that bacterial inhibition strength may be predictable based on Batrachochytrium relatedness. We conclude that bacterial inhibition capabilities change among bacterial strains, Batrachochytrium genotypes and temperatures. A comprehensive understanding of bacterial inhibitory function, across pathogen genotypes and temperatures, is needed to better predict the role of bacterial symbionts in amphibian disease ecology. For targeted conservation applications, we recommend using bacterial strains identified as strongly inhibitory as they are most likely to produce broad-spectrum antimicrobial agents at a range of temperatures.
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spelling doaj.art-8135ca74bbf14e969db808292b06eb402022-12-22T03:20:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-08-01810.3389/fmicb.2017.01551291948Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin BacteriaCarly R. Muletz-Wolz0Carly R. Muletz-Wolz1Jose G. Almario2Samuel E. Barnett3Samuel E. Barnett4Graziella V. DiRenzo5Graziella V. DiRenzo6An Martel7Frank Pasmans8Kelly R. Zamudio9Luís Felipe Toledo10Karen R. Lips11Department of Biology, University of Maryland, College ParkMD, United StatesCenter for Conservation Genomics, Smithsonian Conservation Biology Institute, National Zoological Park, WashingtonDC, United StatesDepartment of Biology, University of Maryland, College ParkMD, United StatesDepartment of Biology, University of Maryland, College ParkMD, United StatesDepartment of Microbiology, Cornell University, IthacaNY, United StatesDepartment of Biology, University of Maryland, College ParkMD, United StatesDepartment of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa BarbaraCA, United StatesDepartment of Pathology, Bacteriology and Poultry Diseases, Ghent UniversityGhent, BelgiumDepartment of Pathology, Bacteriology and Poultry Diseases, Ghent UniversityGhent, BelgiumDepartment of Ecology and Evolutionary Biology, Cornell University, IthacaNY, United StatesDepartment of Animal Biology, State University of CampinasCampinas, BrazilDepartment of Biology, University of Maryland, College ParkMD, United StatesSymbiotic bacteria may dampen the impacts of infectious diseases on hosts by inhibiting pathogen growth. However, our understanding of the generality of pathogen inhibition by different bacterial taxa across pathogen genotypes and environmental conditions is limited. Bacterial inhibitory properties are of particular interest for the amphibian-killing fungal pathogens (Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans), for which probiotic applications as conservation strategies have been proposed. We quantified the inhibition strength of five putatively B. dendrobatidis-inhibitory bacteria isolated from woodland salamander skin against six Batrachochytrium genotypes at two temperatures (12 and 18°C). We selected six genotypes from across the Batrachochytrium phylogeny: B. salamandrivorans, B. dendrobatidis-Brazil and four genotypes of the B. dendrobatidis Global Panzootic Lineage (GPL1: JEL647, JEL404; GPL2: SRS810, JEL423). We performed 96-well plate challenge assays in a full factorial design. We detected a Batrachochytrium genotype by temperature interaction on bacterial inhibition score for all bacteria, indicating that bacteria vary in ability to inhibit Batrachochytrium depending on pathogen genotype and temperature. Acinetobacter rhizosphaerae moderately inhibited B. salamandrivorans at both temperatures (μ = 46–53%), but not any B. dendrobatidis genotypes. Chryseobacterium sp. inhibited three Batrachochytrium genotypes at both temperatures (μ = 5–71%). Pseudomonas sp. strain 1 inhibited all Batrachochytrium genotypes at 12°C and four Batrachochytrium genotypes at 18°C (μ = 5–100%). Pseudomonas sp. strain 2 and Stenotrophomonas sp. moderately to strongly inhibited all six Batrachochytrium genotypes at both temperatures (μ = 57–100%). All bacteria consistently inhibited B. salamandrivorans. Using cluster analysis of inhibition scores, we found that more closely related Batrachochytrium genotypes grouped together, suggesting that bacterial inhibition strength may be predictable based on Batrachochytrium relatedness. We conclude that bacterial inhibition capabilities change among bacterial strains, Batrachochytrium genotypes and temperatures. A comprehensive understanding of bacterial inhibitory function, across pathogen genotypes and temperatures, is needed to better predict the role of bacterial symbionts in amphibian disease ecology. For targeted conservation applications, we recommend using bacterial strains identified as strongly inhibitory as they are most likely to produce broad-spectrum antimicrobial agents at a range of temperatures.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01551/fullsymbiontsalamanderBatrachochytriumantifungaldisease ecology
spellingShingle Carly R. Muletz-Wolz
Carly R. Muletz-Wolz
Jose G. Almario
Samuel E. Barnett
Samuel E. Barnett
Graziella V. DiRenzo
Graziella V. DiRenzo
An Martel
Frank Pasmans
Kelly R. Zamudio
Luís Felipe Toledo
Karen R. Lips
Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria
Frontiers in Microbiology
symbiont
salamander
Batrachochytrium
antifungal
disease ecology
title Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria
title_full Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria
title_fullStr Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria
title_full_unstemmed Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria
title_short Inhibition of Fungal Pathogens across Genotypes and Temperatures by Amphibian Skin Bacteria
title_sort inhibition of fungal pathogens across genotypes and temperatures by amphibian skin bacteria
topic symbiont
salamander
Batrachochytrium
antifungal
disease ecology
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01551/full
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