Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease.
Microbial communities can augment host immune responses and probiotic therapies are under development to prevent or treat diseases of humans, crops, livestock, and wildlife including an emerging fungal disease of amphibians, chytridiomycosis. However, little is known about the stability of host-associated microbiota, or how the microbiota is structured by innate immune factors including antimicrobial peptides (AMPs) abundant in the skin secretions of many amphibians. Thus, conservation medicine including therapies targeting the skin will benefit from investigations of amphibian microbial ecology that provide a model for vertebrate host-symbiont interactions on mucosal surfaces. Here, we tested whether the cutaneous microbiota of Panamanian rocket frogs, Colostethus panamansis, was resistant to colonization or altered by treatment. Under semi-natural outdoor mesocosm conditions in Panama, we exposed frogs to one of three treatments including: (1) probiotic - the potentially beneficial bacterium Lysinibacillus fusiformis, (2) transplant - skin washes from the chytridiomycosis-resistant glass frog Espadarana prosoblepon, and (3) control - sterile water. Microbial assemblages were analyzed by a culture-independent T-RFLP analysis. We found that skin microbiota of C. panamansis was resistant to colonization and did not differ among treatments, but shifted through time in the mesocosms. We describe regulation of host AMPs that may function to maintain microbial community stability. Colonization resistance was metabolically costly and microbe-treated frogs lost 7-12% of body mass. The discovery of strong colonization resistance of skin microbiota suggests a well-regulated, rather than dynamic, host-symbiont relationship, and suggests that probiotic therapies aiming to enhance host immunity may require an approach that circumvents host mechanisms maintaining equilibrium in microbial communities.
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
Denise
D
Küng
Institute of Organic Chemistry, University of Zurich, Zurich, Switzerland.
Laurent
L
Bigler
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
Leyla R
LR
Davis
Center for Species Survival, Conservation and Science, National Zoological Park, Smithsonian Institution, Washington DC, United States of America.
Brian
B
Gratwicke
El Valle Amphibian Conservation Center, El Valle, República de Panamá
Edgardo
E
Griffith
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland ; Smithsonian Tropical Research Institute, Balboa, Ancón, Panamá, República de Panamá
Douglas C
DC
Woodhams
D029845:Amphibian Proteins / Q000502:physiology; D000818:Animals; D023181:Antimicrobial Cationic Peptides / Q000502:physiology; D001001:Anura / Q000276:immunology* / Q000382:microbiology; D001407:Bacillus / Q000502:physiology*; D008411:Chytridiomycota / Q000276:immunology*; D003881:Dermatomycoses / Q000276:immunology / Q000662:veterinary*; D060467:Disease Resistance; D054884:Host-Pathogen Interactions; D064307:Microbiota / Q000276:immunology*; D019936:Probiotics; D012867:Skin / Q000378:metabolism / Q000382:microbiology; D015431:Weight Loss / Q000276:immunology
D029845:Amphibian Proteins; D023181:Antimicrobial Cationic Peptides