The skin microbiome facilitates adaptive tetrodotoxin production in poisonous newts

Autor: Lauren A. O’Connell, James A. Foster, Janet E Williams, Heather L. Eisthen, Patric M Vaelli, Kevin R. Theis
Rok vydání: 2020
Předmět:
Male
0301 basic medicine
chemistry.chemical_compound
Biology (General)
Animals
Poisonous

Skin
education.field_of_study
biology
Microbiota
musculoskeletal
neural
and ocular physiology

General Neuroscience
General Medicine
Adaptation
Physiological

Sphingopyxis
embryonic structures
Tetrodotoxin
Medicine
Chemical defense
Research Article
Symbiotic bacteria
Amphibian
animal structures
QH301-705.5
Science
Population
Zoology
Context (language use)
TTX
autoresistance
General Biochemistry
Genetics and Molecular Biology

03 medical and health sciences
biology.animal
Animals
Symbiosis
education
Evolutionary Biology
Bacteria
030102 biochemistry & molecular biology
General Immunology and Microbiology
urogenital system
neurotoxin
Salamandridae
biology.organism_classification
Culture Media
body regions
030104 developmental biology
chemistry
Predatory Behavior
ion channel
Taricha
taricha granulosa
amphibian
Other
Zdroj: eLife
eLife, Vol 9 (2020)
ISSN: 2050-084X
DOI: 10.7554/elife.53898
Popis: Rough-skinned newts (Taricha granulosa) use tetrodotoxin (TTX) to block voltage-gated sodium (Nav) channels as a chemical defense against predation. Interestingly, newts exhibit extreme population-level variation in toxicity attributed to a coevolutionary arms race with TTX-resistant predatory snakes, but the source of TTX in newts is unknown. Here, we investigated whether symbiotic bacteria isolated from toxic newts could produce TTX. We characterized the skin-associated microbiota from a toxic and non-toxic population of newts and established pure cultures of isolated bacterial symbionts from toxic newts. We then screened bacterial culture media for TTX using LC-MS/MS and identified TTX-producing bacterial strains from four genera, including Aeromonas, Pseudomonas, Shewanella, and Sphingopyxis. Additionally, we sequenced the Nav channel gene family in toxic newts and found that newts expressed Nav channels with modified TTX binding sites, conferring extreme physiological resistance to TTX. This study highlights the complex interactions among adaptive physiology, animal-bacterial symbiosis, and ecological context.
eLife digest Rough-skinned newts produce tetrodotoxin or TTX, a deadly neurotoxin that is also present in some pufferfish, octopuses, crabs, starfish, flatworms, frogs, and toads. It remains a mystery why so many different creatures produce this toxin. One possibility is that TTX did not evolve in animals at all, but rather it is made by bacteria living on or in these creatures. In fact, scientists have already shown that TTX-producing bacteria supply pufferfish, octopus, and other animals with the toxin. However, it was not known where TTX in newts and other amphibians comes from. TTX kills animals by blocking specialized ion channels and shutting down the signaling between neurons, but rough-skinned newts appear insensitive to this blockage, making it likely that they have evolved defenses against the toxin. Some garter snakes that feed on these newts have also evolved to become immune to the effects of TTX. If bacteria are the source of TTX in the newts, the emergence of newt-eating snakes resistant to TTX must be putting evolutionary pressure on both the newts and the bacteria to boost their anti-snake defenses. Learning more about these complex relationships will help scientists better understand both evolution and the role of beneficial bacteria. Vaelli et al. have now shown that bacteria living on rough-skinned newts produce TTX. In the experiments, bacteria samples were collected from the skin of the newts and grown in the laboratory. Four different types of bacteria from the samples collected produced TTX. Next, Vaelli et al. looked at five genes that encode the channels normally affected by TTX in newts and found that all them have mutations that prevent them from being blocked by this deadly neurotoxin. This suggests that bacteria living on newts shape the evolution of genes critical to the animals’ own survival. Helpful bacteria living on and in animals have important effects on animals’ physiology, health, and disease. But understanding these complex interactions is challenging. Rough-skinned newts provide an excellent model system for studying the effects of helpful bacteria living on animals. Vaelli et al. show that a single chemical produced by bacteria can impact diverse aspects of animal biology including physiology, the evolution of their genes, and their interactions with other creatures in their environment.
Databáze: OpenAIRE