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Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter

BACKGROUND: Microbiome in early life has long-term effects on the host’s immunological and physiological development and its disturbance is known to trigger various diseases in host Deuterostome animals. The sea cucumber Apostichopus japonicus is one of the most valuable marine Deuterostome inverteb...

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Autores principales: Yu, Juanwen, Jiang, Chunqi, Yamano, Ryota, Koike, Shotaro, Sakai, Yuichi, Mino, Sayaka, Sawabe, Tomoo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10599069/
https://www.ncbi.nlm.nih.gov/pubmed/37876012
http://dx.doi.org/10.1186/s42523-023-00276-2
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author Yu, Juanwen
Jiang, Chunqi
Yamano, Ryota
Koike, Shotaro
Sakai, Yuichi
Mino, Sayaka
Sawabe, Tomoo
author_facet Yu, Juanwen
Jiang, Chunqi
Yamano, Ryota
Koike, Shotaro
Sakai, Yuichi
Mino, Sayaka
Sawabe, Tomoo
author_sort Yu, Juanwen
collection PubMed
description BACKGROUND: Microbiome in early life has long-term effects on the host’s immunological and physiological development and its disturbance is known to trigger various diseases in host Deuterostome animals. The sea cucumber Apostichopus japonicus is one of the most valuable marine Deuterostome invertebrates in Asia and a model animal in regeneration studies. To understand factors that impact on host development and holobiont maintenance, host-microbiome association has been actively studied in the last decade. However, we currently lack knowledge of early life core microbiome during its ontogenesis and how it benefits the host’s growth. RESULTS: We analyzed the microbial community in 28 sea cucumber samples from a laboratory breeding system, designed to replicate aquaculture environments, across six developmental stages (fertilized eggs to the juvenile stage) over a three years-period to examine the microbiomes’ dynamics and stability. Microbiome shifts occurred during sea cucumber larval ontogenesis in every case. Application of the most sophisticated core microbiome extraction methodology, a hybrid approach with abundance-occupancy core microbiome analyses (top 75% of total reads and > 70% occupation) and core index calculation, first revealed early life core microbiome consisted of Alteromonadaceae and Rhodobacteraceae, as well as a stage core microbiome consisting of pioneer core microbe Pseudoalteromonadaceae in A. japonicus, suggesting a stepwise establishment of microbiome related to ontogenesis and feeding behavior in A. japonicus. More interestingly, four ASVs affiliated to Alteromonadaceae and Rhodobacteraceae were extracted as early life core microbiome. One of the ASV (ASV0007) was affiliated to the Sulfitobactor strain BL28 (Rhodobacteraceae), isolated from blastula larvae in the 2019 raring batch. Unexpectedly, a bioassay revealed the BL28 strain retains a host growth-promoting ability. Further meta-pangenomics approach revealed the BL28 genome reads were abundant in the metagenomic sequence pool, in particular, in that of post-gut development in early life stages of A. japonicus. CONCLUSION: Repeated rearing efforts of A. japonicus using laboratory aquaculture replicating aquaculture environments and hybrid core microbiome extraction approach first revealed particular ASVs affiliated to Alteromonadaceae and Rhodobacteraceae as the A. japonicus early life core microbiome. Further bioassay revealed the growth promoting ability to the host sea cucumber in one of the core microbes, the Sulfitobactor strain BL28 identified as ASV0007. Genome reads of the BL28 were abundant in post-gut development of A. japonicus, which makes us consider effective probiotic uses of those core microbiome for sea cucumber resource production and conservation. The study also emphasizes the importance of the core microbiome in influencing early life stages in marine invertebrates. Understanding these dynamics could offer pathways to improve growth, immunity, and disease resistance in marine invertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00276-2.
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spelling pubmed-105990692023-10-26 Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter Yu, Juanwen Jiang, Chunqi Yamano, Ryota Koike, Shotaro Sakai, Yuichi Mino, Sayaka Sawabe, Tomoo Anim Microbiome Research BACKGROUND: Microbiome in early life has long-term effects on the host’s immunological and physiological development and its disturbance is known to trigger various diseases in host Deuterostome animals. The sea cucumber Apostichopus japonicus is one of the most valuable marine Deuterostome invertebrates in Asia and a model animal in regeneration studies. To understand factors that impact on host development and holobiont maintenance, host-microbiome association has been actively studied in the last decade. However, we currently lack knowledge of early life core microbiome during its ontogenesis and how it benefits the host’s growth. RESULTS: We analyzed the microbial community in 28 sea cucumber samples from a laboratory breeding system, designed to replicate aquaculture environments, across six developmental stages (fertilized eggs to the juvenile stage) over a three years-period to examine the microbiomes’ dynamics and stability. Microbiome shifts occurred during sea cucumber larval ontogenesis in every case. Application of the most sophisticated core microbiome extraction methodology, a hybrid approach with abundance-occupancy core microbiome analyses (top 75% of total reads and > 70% occupation) and core index calculation, first revealed early life core microbiome consisted of Alteromonadaceae and Rhodobacteraceae, as well as a stage core microbiome consisting of pioneer core microbe Pseudoalteromonadaceae in A. japonicus, suggesting a stepwise establishment of microbiome related to ontogenesis and feeding behavior in A. japonicus. More interestingly, four ASVs affiliated to Alteromonadaceae and Rhodobacteraceae were extracted as early life core microbiome. One of the ASV (ASV0007) was affiliated to the Sulfitobactor strain BL28 (Rhodobacteraceae), isolated from blastula larvae in the 2019 raring batch. Unexpectedly, a bioassay revealed the BL28 strain retains a host growth-promoting ability. Further meta-pangenomics approach revealed the BL28 genome reads were abundant in the metagenomic sequence pool, in particular, in that of post-gut development in early life stages of A. japonicus. CONCLUSION: Repeated rearing efforts of A. japonicus using laboratory aquaculture replicating aquaculture environments and hybrid core microbiome extraction approach first revealed particular ASVs affiliated to Alteromonadaceae and Rhodobacteraceae as the A. japonicus early life core microbiome. Further bioassay revealed the growth promoting ability to the host sea cucumber in one of the core microbes, the Sulfitobactor strain BL28 identified as ASV0007. Genome reads of the BL28 were abundant in post-gut development of A. japonicus, which makes us consider effective probiotic uses of those core microbiome for sea cucumber resource production and conservation. The study also emphasizes the importance of the core microbiome in influencing early life stages in marine invertebrates. Understanding these dynamics could offer pathways to improve growth, immunity, and disease resistance in marine invertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00276-2. BioMed Central 2023-10-24 /pmc/articles/PMC10599069/ /pubmed/37876012 http://dx.doi.org/10.1186/s42523-023-00276-2 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 Research
Yu, Juanwen
Jiang, Chunqi
Yamano, Ryota
Koike, Shotaro
Sakai, Yuichi
Mino, Sayaka
Sawabe, Tomoo
Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter
title Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter
title_full Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter
title_fullStr Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter
title_full_unstemmed Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter
title_short Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter
title_sort unveiling the early life core microbiome of the sea cucumber apostichopus japonicus and the unexpected abundance of the growth-promoting sulfitobacter
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10599069/
https://www.ncbi.nlm.nih.gov/pubmed/37876012
http://dx.doi.org/10.1186/s42523-023-00276-2
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