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Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling

Xenopus laevis tadpoles can regenerate functional tails, containing the spinal cord, notochord, muscle, fin, blood vessels and nerves, except for a brief refractory period at around 1 week of age. At this stage, amputation of the tadpole's tail may either result in scarless wound healing or the...

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Autores principales: Chapman, Phoebe A., Gilbert, Campbell B., Devine, Thomas J., Hudson, Daniel T., Ward, Joanna, Morgan, Xochitl C., Beck, Caroline W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9790228/
https://www.ncbi.nlm.nih.gov/pubmed/35212086
http://dx.doi.org/10.1111/wrr.13003
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author Chapman, Phoebe A.
Gilbert, Campbell B.
Devine, Thomas J.
Hudson, Daniel T.
Ward, Joanna
Morgan, Xochitl C.
Beck, Caroline W.
author_facet Chapman, Phoebe A.
Gilbert, Campbell B.
Devine, Thomas J.
Hudson, Daniel T.
Ward, Joanna
Morgan, Xochitl C.
Beck, Caroline W.
author_sort Chapman, Phoebe A.
collection PubMed
description Xenopus laevis tadpoles can regenerate functional tails, containing the spinal cord, notochord, muscle, fin, blood vessels and nerves, except for a brief refractory period at around 1 week of age. At this stage, amputation of the tadpole's tail may either result in scarless wound healing or the activation of a regeneration programme, which replaces the lost tissues. We recently demonstrated a link between bacterial lipopolysaccharides and successful tail regeneration in refractory stage tadpoles and proposed that this could result from lipopolysaccharides binding to Toll‐like receptor 4 (TLR4). Here, we have used 16S rRNA sequencing to show that the tadpole skin microbiome is highly variable between sibships and that the community can be altered by raising embryos in the antibiotic gentamicin. Six Gram‐negative genera, including Delftia and Chryseobacterium, were over‐represented in tadpoles that underwent tail regeneration. Lipopolysaccharides purified from a commensal Chryseobacterium spp. XDS4, an exogenous Delftia spp. or Escherichia coli, could significantly increase the number of antibiotic‐raised tadpoles that attempted regeneration. Conversely, the quality of regeneration was impaired in native‐raised tadpoles exposed to the antagonistic lipopolysaccharide of Rhodobacter sphaeroides. Editing TLR4 using CRISPR/Cas9 also reduced regeneration quality, but not quantity, at the level of the cohort. However, we found that the editing level of individual tadpoles was a poor predictor of regenerative outcome. In conclusion, our results suggest that variable regeneration in refractory stage tadpoles depends at least in part on the skin microbiome and lipopolysaccharide signalling, but that signalling via TLR4 cannot account for all of this effect.
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spelling pubmed-97902282022-12-28 Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling Chapman, Phoebe A. Gilbert, Campbell B. Devine, Thomas J. Hudson, Daniel T. Ward, Joanna Morgan, Xochitl C. Beck, Caroline W. Wound Repair Regen Original Article‐Regeneration Science Xenopus laevis tadpoles can regenerate functional tails, containing the spinal cord, notochord, muscle, fin, blood vessels and nerves, except for a brief refractory period at around 1 week of age. At this stage, amputation of the tadpole's tail may either result in scarless wound healing or the activation of a regeneration programme, which replaces the lost tissues. We recently demonstrated a link between bacterial lipopolysaccharides and successful tail regeneration in refractory stage tadpoles and proposed that this could result from lipopolysaccharides binding to Toll‐like receptor 4 (TLR4). Here, we have used 16S rRNA sequencing to show that the tadpole skin microbiome is highly variable between sibships and that the community can be altered by raising embryos in the antibiotic gentamicin. Six Gram‐negative genera, including Delftia and Chryseobacterium, were over‐represented in tadpoles that underwent tail regeneration. Lipopolysaccharides purified from a commensal Chryseobacterium spp. XDS4, an exogenous Delftia spp. or Escherichia coli, could significantly increase the number of antibiotic‐raised tadpoles that attempted regeneration. Conversely, the quality of regeneration was impaired in native‐raised tadpoles exposed to the antagonistic lipopolysaccharide of Rhodobacter sphaeroides. Editing TLR4 using CRISPR/Cas9 also reduced regeneration quality, but not quantity, at the level of the cohort. However, we found that the editing level of individual tadpoles was a poor predictor of regenerative outcome. In conclusion, our results suggest that variable regeneration in refractory stage tadpoles depends at least in part on the skin microbiome and lipopolysaccharide signalling, but that signalling via TLR4 cannot account for all of this effect. John Wiley & Sons, Inc. 2022-02-25 2022 /pmc/articles/PMC9790228/ /pubmed/35212086 http://dx.doi.org/10.1111/wrr.13003 Text en © 2022 The Authors. Wound Repair and Regeneration published by Wiley Periodicals LLC on behalf of The Wound Healing Society. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Article‐Regeneration Science
Chapman, Phoebe A.
Gilbert, Campbell B.
Devine, Thomas J.
Hudson, Daniel T.
Ward, Joanna
Morgan, Xochitl C.
Beck, Caroline W.
Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling
title Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling
title_full Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling
title_fullStr Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling
title_full_unstemmed Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling
title_short Manipulating the microbiome alters regenerative outcomes in Xenopus laevis tadpoles via lipopolysaccharide signalling
title_sort manipulating the microbiome alters regenerative outcomes in xenopus laevis tadpoles via lipopolysaccharide signalling
topic Original Article‐Regeneration Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9790228/
https://www.ncbi.nlm.nih.gov/pubmed/35212086
http://dx.doi.org/10.1111/wrr.13003
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