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High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata

Bacteria commonly form aggregates in a range of coral species [termed coral-associated microbial aggregates (CAMAs)], although these structures remain poorly characterized despite extensive efforts studying the coral microbiome. Here, we comprehensively characterize CAMAs associated with Stylophora...

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Autores principales: Wada, Naohisa, Hsu, Ming-Tsung, Tandon, Kshitij, Hsiao, Silver Sung-Yun, Chen, Hsing-Ju, Chen, Yu-Hsiang, Chiang, Pei-Wen, Yu, Sheng-Ping, Lu, Chih-Ying, Chiou, Yu-Jing, Tu, Yung-Chi, Tian, Xuejiao, Chen, Bi-Chang, Lee, Der-Chuen, Yamashiro, Hideyuki, Bourne, David G., Tang, Sen-Lin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9258956/
https://www.ncbi.nlm.nih.gov/pubmed/35857470
http://dx.doi.org/10.1126/sciadv.abo2431
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author Wada, Naohisa
Hsu, Ming-Tsung
Tandon, Kshitij
Hsiao, Silver Sung-Yun
Chen, Hsing-Ju
Chen, Yu-Hsiang
Chiang, Pei-Wen
Yu, Sheng-Ping
Lu, Chih-Ying
Chiou, Yu-Jing
Tu, Yung-Chi
Tian, Xuejiao
Chen, Bi-Chang
Lee, Der-Chuen
Yamashiro, Hideyuki
Bourne, David G.
Tang, Sen-Lin
author_facet Wada, Naohisa
Hsu, Ming-Tsung
Tandon, Kshitij
Hsiao, Silver Sung-Yun
Chen, Hsing-Ju
Chen, Yu-Hsiang
Chiang, Pei-Wen
Yu, Sheng-Ping
Lu, Chih-Ying
Chiou, Yu-Jing
Tu, Yung-Chi
Tian, Xuejiao
Chen, Bi-Chang
Lee, Der-Chuen
Yamashiro, Hideyuki
Bourne, David G.
Tang, Sen-Lin
author_sort Wada, Naohisa
collection PubMed
description Bacteria commonly form aggregates in a range of coral species [termed coral-associated microbial aggregates (CAMAs)], although these structures remain poorly characterized despite extensive efforts studying the coral microbiome. Here, we comprehensively characterize CAMAs associated with Stylophora pistillata and quantify their cell abundance. Our analysis reveals that multiple Endozoicomonas phylotypes coexist inside a single CAMA. Nanoscale secondary ion mass spectrometry imaging revealed that the Endozoicomonas cells were enriched with phosphorus, with the elemental compositions of CAMAs different from coral tissues and endosymbiotic Symbiodiniaceae, highlighting a role in sequestering and cycling phosphate between coral holobiont partners. Consensus metagenome-assembled genomes of the two dominant Endozoicomonas phylotypes confirmed their metabolic potential for polyphosphate accumulation along with genomic signatures including type VI secretion systems allowing host association. Our findings provide unprecedented insights into Endozoicomonas-dominated CAMAs and the first direct physiological and genomic linked evidence of their biological role in the coral holobiont.
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spelling pubmed-92589562022-07-20 High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata Wada, Naohisa Hsu, Ming-Tsung Tandon, Kshitij Hsiao, Silver Sung-Yun Chen, Hsing-Ju Chen, Yu-Hsiang Chiang, Pei-Wen Yu, Sheng-Ping Lu, Chih-Ying Chiou, Yu-Jing Tu, Yung-Chi Tian, Xuejiao Chen, Bi-Chang Lee, Der-Chuen Yamashiro, Hideyuki Bourne, David G. Tang, Sen-Lin Sci Adv Earth, Environmental, Ecological, and Space Sciences Bacteria commonly form aggregates in a range of coral species [termed coral-associated microbial aggregates (CAMAs)], although these structures remain poorly characterized despite extensive efforts studying the coral microbiome. Here, we comprehensively characterize CAMAs associated with Stylophora pistillata and quantify their cell abundance. Our analysis reveals that multiple Endozoicomonas phylotypes coexist inside a single CAMA. Nanoscale secondary ion mass spectrometry imaging revealed that the Endozoicomonas cells were enriched with phosphorus, with the elemental compositions of CAMAs different from coral tissues and endosymbiotic Symbiodiniaceae, highlighting a role in sequestering and cycling phosphate between coral holobiont partners. Consensus metagenome-assembled genomes of the two dominant Endozoicomonas phylotypes confirmed their metabolic potential for polyphosphate accumulation along with genomic signatures including type VI secretion systems allowing host association. Our findings provide unprecedented insights into Endozoicomonas-dominated CAMAs and the first direct physiological and genomic linked evidence of their biological role in the coral holobiont. American Association for the Advancement of Science 2022-07-06 /pmc/articles/PMC9258956/ /pubmed/35857470 http://dx.doi.org/10.1126/sciadv.abo2431 Text en Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Earth, Environmental, Ecological, and Space Sciences
Wada, Naohisa
Hsu, Ming-Tsung
Tandon, Kshitij
Hsiao, Silver Sung-Yun
Chen, Hsing-Ju
Chen, Yu-Hsiang
Chiang, Pei-Wen
Yu, Sheng-Ping
Lu, Chih-Ying
Chiou, Yu-Jing
Tu, Yung-Chi
Tian, Xuejiao
Chen, Bi-Chang
Lee, Der-Chuen
Yamashiro, Hideyuki
Bourne, David G.
Tang, Sen-Lin
High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata
title High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata
title_full High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata
title_fullStr High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata
title_full_unstemmed High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata
title_short High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata
title_sort high-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral stylophora pistillata
topic Earth, Environmental, Ecological, and Space Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9258956/
https://www.ncbi.nlm.nih.gov/pubmed/35857470
http://dx.doi.org/10.1126/sciadv.abo2431
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