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Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish

The bioluminescent symbiosis involving the urchin cardinalfish, Siphamia tubifer, and Photobacterium mandapamensis, a luminous member of the Vibrionaceae, is highly specific compared to other bioluminescent fish-bacteria associations. Despite this high degree of specificity, patterns of genetic dive...

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Autores principales: Gould, A. L., Donohoo, S. A., Román, E. D., Neff, E. E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689835/
https://www.ncbi.nlm.nih.gov/pubmed/37891426
http://dx.doi.org/10.1038/s41396-023-01550-6
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author Gould, A. L.
Donohoo, S. A.
Román, E. D.
Neff, E. E.
author_facet Gould, A. L.
Donohoo, S. A.
Román, E. D.
Neff, E. E.
author_sort Gould, A. L.
collection PubMed
description The bioluminescent symbiosis involving the urchin cardinalfish, Siphamia tubifer, and Photobacterium mandapamensis, a luminous member of the Vibrionaceae, is highly specific compared to other bioluminescent fish-bacteria associations. Despite this high degree of specificity, patterns of genetic diversity have been observed for the symbionts from hosts sampled over relatively small spatial scales. We characterized and compared sub-species, strain-level symbiont diversity within and between S. tubifer hosts sampled from the Philippines and Japan using PCR fingerprinting. We then carried out whole genome sequencing of the unique symbiont genotypes identified to characterize the genetic diversity of the symbiont community and the symbiont pangenome. We determined that an individual light organ contains six symbiont genotypes on average, but varied between 1–13. Additionally, we found that there were few genotypes shared between hosts from the same location. A phylogenetic analysis of the unique symbiont strains indicated location-specific clades, suggesting some genetic differentiation in the symbionts between host populations. We also identified symbiont genes that were variable between strains, including luxF, a member of the lux operon, which is responsible for light production. We quantified the light emission and growth rate of two strains missing luxF along with the other strains isolated from the same light organs and determined that strains lacking luxF were dimmer but grew faster than most of the other strains, suggesting a potential metabolic trade-off. This study highlights the importance of strain-level diversity in microbial associations and provides new insight into the underlying genetic architecture of intraspecific symbiont communities within a host.
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spelling pubmed-106898352023-12-02 Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish Gould, A. L. Donohoo, S. A. Román, E. D. Neff, E. E. ISME J Article The bioluminescent symbiosis involving the urchin cardinalfish, Siphamia tubifer, and Photobacterium mandapamensis, a luminous member of the Vibrionaceae, is highly specific compared to other bioluminescent fish-bacteria associations. Despite this high degree of specificity, patterns of genetic diversity have been observed for the symbionts from hosts sampled over relatively small spatial scales. We characterized and compared sub-species, strain-level symbiont diversity within and between S. tubifer hosts sampled from the Philippines and Japan using PCR fingerprinting. We then carried out whole genome sequencing of the unique symbiont genotypes identified to characterize the genetic diversity of the symbiont community and the symbiont pangenome. We determined that an individual light organ contains six symbiont genotypes on average, but varied between 1–13. Additionally, we found that there were few genotypes shared between hosts from the same location. A phylogenetic analysis of the unique symbiont strains indicated location-specific clades, suggesting some genetic differentiation in the symbionts between host populations. We also identified symbiont genes that were variable between strains, including luxF, a member of the lux operon, which is responsible for light production. We quantified the light emission and growth rate of two strains missing luxF along with the other strains isolated from the same light organs and determined that strains lacking luxF were dimmer but grew faster than most of the other strains, suggesting a potential metabolic trade-off. This study highlights the importance of strain-level diversity in microbial associations and provides new insight into the underlying genetic architecture of intraspecific symbiont communities within a host. Nature Publishing Group UK 2023-10-27 2023-12 /pmc/articles/PMC10689835/ /pubmed/37891426 http://dx.doi.org/10.1038/s41396-023-01550-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Gould, A. L.
Donohoo, S. A.
Román, E. D.
Neff, E. E.
Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
title Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
title_full Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
title_fullStr Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
title_full_unstemmed Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
title_short Strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
title_sort strain-level diversity of symbiont communities between individuals and populations of a bioluminescent fish
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689835/
https://www.ncbi.nlm.nih.gov/pubmed/37891426
http://dx.doi.org/10.1038/s41396-023-01550-6
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