Literature DB >> 27655769

Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity.

Jordan G Kueneman1, Douglas C Woodhams1, Reid Harris2, Holly M Archer1, Rob Knight3, Valerie J McKenzie4.   

Abstract

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.
© 2016 The Author(s).

Entities:  

Keywords:  Anaxyrus boreas; Batrachochytrium dendrobatidis; amphibian; captivity; microbiome; probiotics

Mesh:

Year:  2016        PMID: 27655769      PMCID: PMC5046908          DOI: 10.1098/rspb.2016.1553

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  26 in total

Review 1.  Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use.

Authors:  Molly C Bletz; Andrew H Loudon; Matthew H Becker; Sara C Bell; Douglas C Woodhams; Kevin P C Minbiole; Reid N Harris
Journal:  Ecol Lett       Date:  2013-03-03       Impact factor: 9.492

2.  The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus.

Authors:  Matthew H Becker; Robert M Brucker; Christian R Schwantes; Reid N Harris; Kevin P C Minbiole
Journal:  Appl Environ Microbiol       Date:  2009-08-28       Impact factor: 4.792

3.  Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus.

Authors:  Reid N Harris; Robert M Brucker; Jenifer B Walke; Matthew H Becker; Christian R Schwantes; Devon C Flaherty; Brianna A Lam; Douglas C Woodhams; Cheryl J Briggs; Vance T Vredenburg; Kevin P C Minbiole
Journal:  ISME J       Date:  2009-03-26       Impact factor: 10.302

4.  Inhibitory bacteria reduce fungi on early life stages of endangered Colorado boreal toads (Anaxyrus boreas).

Authors:  Jordan G Kueneman; Douglas C Woodhams; Will Van Treuren; Holly M Archer; Rob Knight; Valerie J McKenzie
Journal:  ISME J       Date:  2015-11-13       Impact factor: 10.302

5.  Co-habiting amphibian species harbor unique skin bacterial communities in wild populations.

Authors:  Valerie J McKenzie; Robert M Bowers; Noah Fierer; Rob Knight; Christian L Lauber
Journal:  ISME J       Date:  2011-09-29       Impact factor: 10.302

6.  Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus).

Authors:  Andrew H Loudon; Douglas C Woodhams; Laura Wegener Parfrey; Holly Archer; Rob Knight; Valerie McKenzie; Reid N Harris
Journal:  ISME J       Date:  2013-12-12       Impact factor: 10.302

7.  Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness.

Authors:  Douglas C Woodhams; Hannelore Brandt; Simone Baumgartner; Jos Kielgast; Eliane Küpfer; Ursina Tobler; Leyla R Davis; Benedikt R Schmidt; Christian Bel; Sandro Hodel; Rob Knight; Valerie McKenzie
Journal:  PLoS One       Date:  2014-04-30       Impact factor: 3.240

Review 8.  Using "Omics" and Integrated Multi-Omics Approaches to Guide Probiotic Selection to Mitigate Chytridiomycosis and Other Emerging Infectious Diseases.

Authors:  Eria A Rebollar; Rachael E Antwis; Matthew H Becker; Lisa K Belden; Molly C Bletz; Robert M Brucker; Xavier A Harrison; Myra C Hughey; Jordan G Kueneman; Andrew H Loudon; Valerie McKenzie; Daniel Medina; Kevin P C Minbiole; Louise A Rollins-Smith; Jenifer B Walke; Sophie Weiss; Douglas C Woodhams; Reid N Harris
Journal:  Front Microbiol       Date:  2016-02-02       Impact factor: 5.640

9.  Community Structure and Function of Amphibian Skin Microbes: An Experiment with Bullfrogs Exposed to a Chytrid Fungus.

Authors:  Jenifer B Walke; Matthew H Becker; Stephen C Loftus; Leanna L House; Thais L Teotonio; Kevin P C Minbiole; Lisa K Belden
Journal:  PLoS One       Date:  2015-10-07       Impact factor: 3.240

10.  Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences.

Authors:  Jai Ram Rideout; Yan He; Jose A Navas-Molina; William A Walters; Luke K Ursell; Sean M Gibbons; John Chase; Daniel McDonald; Antonio Gonzalez; Adam Robbins-Pianka; Jose C Clemente; Jack A Gilbert; Susan M Huse; Hong-Wei Zhou; Rob Knight; J Gregory Caporaso
Journal:  PeerJ       Date:  2014-08-21       Impact factor: 2.984

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  46 in total

1.  Identification of Bufadienolides from the Boreal Toad, Anaxyrus boreas, Active Against a Fungal Pathogen.

Authors:  Kelly Barnhart; Megan E Forman; Thomas P Umile; Jordan Kueneman; Valerie McKenzie; Irene Salinas; Kevin P C Minbiole; Douglas C Woodhams
Journal:  Microb Ecol       Date:  2017-06-19       Impact factor: 4.552

2.  Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale.

Authors:  Andrea J Jani; Roland A Knapp; Cheryl J Briggs
Journal:  Proc Biol Sci       Date:  2017-06-28       Impact factor: 5.349

3.  Nisin Z produced by Lactococcus lactis from bullfrog hatchery is active against Citrobacter freundii, a red-leg syndrome related pathogen.

Authors:  Gabriel Quintana; Maria V Niederle; Carlos J Minahk; Gianluca Picariello; María E F Nader-Macías; Sergio E Pasteris
Journal:  World J Microbiol Biotechnol       Date:  2017-09-27       Impact factor: 3.312

4.  Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense.

Authors:  Sasha E Greenspan; Mariana L Lyra; Gustavo H Migliorini; Mônica F Kersch-Becker; Molly C Bletz; Cybele Sabino Lisboa; Mariana R Pontes; Luisa P Ribeiro; Wesley J Neely; Felipe Rezende; Gustavo Q Romero; Douglas C Woodhams; Célio F B Haddad; Luís Felipe Toledo; C Guilherme Becker
Journal:  Proc Biol Sci       Date:  2019-06-26       Impact factor: 5.349

Review 5.  Engineering the microbiome for animal health and conservation.

Authors:  Se Jin Song; Douglas C Woodhams; Cameron Martino; Celeste Allaband; Andre Mu; Sandrine Javorschi-Miller-Montgomery; Jan S Suchodolski; Rob Knight
Journal:  Exp Biol Med (Maywood)       Date:  2019-02-18

6.  Functional Redundancy of Batrachochytrium dendrobatidis Inhibition in Bacterial Communities Isolated from Lithobates clamitans Skin.

Authors:  Ariel Kruger
Journal:  Microb Ecol       Date:  2019-06-04       Impact factor: 4.552

7.  Probiotics Modulate a Novel Amphibian Skin Defense Peptide That Is Antifungal and Facilitates Growth of Antifungal Bacteria.

Authors:  Douglas C Woodhams; Louise A Rollins-Smith; Laura K Reinert; Briana A Lam; Reid N Harris; Cheryl J Briggs; Vance T Vredenburg; Bhumi T Patel; Richard M Caprioli; Pierre Chaurand; Peter Hunziker; Laurent Bigler
Journal:  Microb Ecol       Date:  2019-05-16       Impact factor: 4.552

8.  Amphibian skin microbiota exhibits temporal variation in community structure but stability of predicted Bd-inhibitory function.

Authors:  Molly C Bletz; R G Bina Perl; Bianca Tc Bobowski; Laura M Japke; Christoph C Tebbe; Anja B Dohrmann; Sabin Bhuju; Robert Geffers; Michael Jarek; Miguel Vences
Journal:  ISME J       Date:  2017-04-07       Impact factor: 10.302

9.  Microbiota and skin defense peptides may facilitate coexistence of two sympatric Andean frog species with a lethal pathogen.

Authors:  Sandra V Flechas; Alejandro Acosta-González; Laura A Escobar; Jordan G Kueneman; Zilpa Adriana Sánchez-Quitian; Claudia M Parra-Giraldo; Louise A Rollins-Smith; Laura K Reinert; Vance T Vredenburg; Adolfo Amézquita; Douglas C Woodhams
Journal:  ISME J       Date:  2018-09-25       Impact factor: 10.302

Review 10.  The call of the wild: using non-model systems to investigate microbiome-behaviour relationships.

Authors:  Jessica A Cusick; Cara L Wellman; Gregory E Demas
Journal:  J Exp Biol       Date:  2021-05-14       Impact factor: 3.312

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