Cargando…

Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral

BACKGROUND: Endozoicomonas bacteria symbiosis with various marine organisms is hypothesized as a potential indicator of health in corals. Although many amplicon analyses using 16S rRNA gene have suggested the diversity of Endozoicomonas species, genome analysis has been limited due to contamination...

Descripción completa

Detalles Bibliográficos
Autores principales: Ide, Keigo, Nishikawa, Yohei, Maruyama, Toru, Tsukada, Yuko, Kogawa, Masato, Takeda, Hiroki, Ito, Haruka, Wagatsuma, Ryota, Miyaoka, Rimi, Nakano, Yoshikatsu, Kinjo, Koji, Ito, Michihiro, Hosokawa, Masahito, Yura, Kei, Suda, Shoichiro, Takeyama, Haruko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9743535/
https://www.ncbi.nlm.nih.gov/pubmed/36503599
http://dx.doi.org/10.1186/s40168-022-01395-9
_version_ 1784848743187611648
author Ide, Keigo
Nishikawa, Yohei
Maruyama, Toru
Tsukada, Yuko
Kogawa, Masato
Takeda, Hiroki
Ito, Haruka
Wagatsuma, Ryota
Miyaoka, Rimi
Nakano, Yoshikatsu
Kinjo, Koji
Ito, Michihiro
Hosokawa, Masahito
Yura, Kei
Suda, Shoichiro
Takeyama, Haruko
author_facet Ide, Keigo
Nishikawa, Yohei
Maruyama, Toru
Tsukada, Yuko
Kogawa, Masato
Takeda, Hiroki
Ito, Haruka
Wagatsuma, Ryota
Miyaoka, Rimi
Nakano, Yoshikatsu
Kinjo, Koji
Ito, Michihiro
Hosokawa, Masahito
Yura, Kei
Suda, Shoichiro
Takeyama, Haruko
author_sort Ide, Keigo
collection PubMed
description BACKGROUND: Endozoicomonas bacteria symbiosis with various marine organisms is hypothesized as a potential indicator of health in corals. Although many amplicon analyses using 16S rRNA gene have suggested the diversity of Endozoicomonas species, genome analysis has been limited due to contamination of host-derived sequences and difficulties in culture and metagenomic analysis. Therefore, the evolutionary and functional potential of individual Endozoicomonas species symbiotic with the same coral species remains unresolved. RESULTS: In this study, we applied a novel single-cell genomics technique using droplet microfluidics to obtain single-cell amplified genomes (SAGs) for uncultured coral-associated Endozoicomonas spp. We obtained seven novel Endozoicomonas genomes and quantitative bacterial composition from Acropora tenuis corals at four sites in Japan. Our quantitative 16S rRNA gene and comparative genomic analysis revealed that these Endozoicomonas spp. belong to different lineages (Clade A and Clade B), with widely varying abundance among individual corals. Furthermore, each Endozoicomonas species possessed various eukaryotic-like genes in clade-specific genes. It was suggested that these eukaryotic-like genes might have a potential ability of different functions in each clade, such as infection of the host coral or suppression of host immune pathways. These Endozoicomonas species may have adopted different host adaptation strategies despite living symbiotically on the same coral. CONCLUSIONS: This study suggests that coral-associated Endozoicomonas spp. on the same species of coral have different evolutional strategies and functional potentials in each species and emphasizes the need to analyze the genome of each uncultured strain in future coral-Endozoicomonas relationships studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01395-9.
format Online
Article
Text
id pubmed-9743535
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-97435352022-12-13 Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral Ide, Keigo Nishikawa, Yohei Maruyama, Toru Tsukada, Yuko Kogawa, Masato Takeda, Hiroki Ito, Haruka Wagatsuma, Ryota Miyaoka, Rimi Nakano, Yoshikatsu Kinjo, Koji Ito, Michihiro Hosokawa, Masahito Yura, Kei Suda, Shoichiro Takeyama, Haruko Microbiome Research BACKGROUND: Endozoicomonas bacteria symbiosis with various marine organisms is hypothesized as a potential indicator of health in corals. Although many amplicon analyses using 16S rRNA gene have suggested the diversity of Endozoicomonas species, genome analysis has been limited due to contamination of host-derived sequences and difficulties in culture and metagenomic analysis. Therefore, the evolutionary and functional potential of individual Endozoicomonas species symbiotic with the same coral species remains unresolved. RESULTS: In this study, we applied a novel single-cell genomics technique using droplet microfluidics to obtain single-cell amplified genomes (SAGs) for uncultured coral-associated Endozoicomonas spp. We obtained seven novel Endozoicomonas genomes and quantitative bacterial composition from Acropora tenuis corals at four sites in Japan. Our quantitative 16S rRNA gene and comparative genomic analysis revealed that these Endozoicomonas spp. belong to different lineages (Clade A and Clade B), with widely varying abundance among individual corals. Furthermore, each Endozoicomonas species possessed various eukaryotic-like genes in clade-specific genes. It was suggested that these eukaryotic-like genes might have a potential ability of different functions in each clade, such as infection of the host coral or suppression of host immune pathways. These Endozoicomonas species may have adopted different host adaptation strategies despite living symbiotically on the same coral. CONCLUSIONS: This study suggests that coral-associated Endozoicomonas spp. on the same species of coral have different evolutional strategies and functional potentials in each species and emphasizes the need to analyze the genome of each uncultured strain in future coral-Endozoicomonas relationships studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01395-9. BioMed Central 2022-12-12 /pmc/articles/PMC9743535/ /pubmed/36503599 http://dx.doi.org/10.1186/s40168-022-01395-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ide, Keigo
Nishikawa, Yohei
Maruyama, Toru
Tsukada, Yuko
Kogawa, Masato
Takeda, Hiroki
Ito, Haruka
Wagatsuma, Ryota
Miyaoka, Rimi
Nakano, Yoshikatsu
Kinjo, Koji
Ito, Michihiro
Hosokawa, Masahito
Yura, Kei
Suda, Shoichiro
Takeyama, Haruko
Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral
title Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral
title_full Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral
title_fullStr Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral
title_full_unstemmed Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral
title_short Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral
title_sort targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria endozoicomonas in acropora tenuis coral
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9743535/
https://www.ncbi.nlm.nih.gov/pubmed/36503599
http://dx.doi.org/10.1186/s40168-022-01395-9
work_keys_str_mv AT idekeigo targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT nishikawayohei targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT maruyamatoru targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT tsukadayuko targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT kogawamasato targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT takedahiroki targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT itoharuka targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT wagatsumaryota targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT miyaokarimi targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT nakanoyoshikatsu targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT kinjokoji targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT itomichihiro targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT hosokawamasahito targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT yurakei targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT sudashoichiro targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral
AT takeyamaharuko targetedsinglecellgenomicsrevealsnovelhostadaptationstrategiesofthesymbioticbacteriaendozoicomonasinacroporatenuiscoral