Changes in the diversity and functionality of viruses that can bleach healthy coral

ABSTRACT Coral microbiomes play a crucial role in maintaining the health and functionality of holobionts. Disruption in the equilibrium of holobionts, including bacteria, fungi, and archaea, can result in the bleaching of coral. However, little is known about the viruses that can infect holobionts i...

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Main Authors: Zhengyi Zhang, Mengmeng Tong, Wei Ding, Shuikai Liu, Mui-Choo Jong, Ahmed A. Radwan, Zhonghua Cai, Jin Zhou
Format: Article
Language:English
Published: American Society for Microbiology 2024-12-01
Series:mSphere
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Online Access:https://journals.asm.org/doi/10.1128/msphere.00816-24
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author Zhengyi Zhang
Mengmeng Tong
Wei Ding
Shuikai Liu
Mui-Choo Jong
Ahmed A. Radwan
Zhonghua Cai
Jin Zhou
author_facet Zhengyi Zhang
Mengmeng Tong
Wei Ding
Shuikai Liu
Mui-Choo Jong
Ahmed A. Radwan
Zhonghua Cai
Jin Zhou
author_sort Zhengyi Zhang
collection DOAJ
description ABSTRACT Coral microbiomes play a crucial role in maintaining the health and functionality of holobionts. Disruption in the equilibrium of holobionts, including bacteria, fungi, and archaea, can result in the bleaching of coral. However, little is known about the viruses that can infect holobionts in coral, especially bacteriophages. Here, we employed a combination of amplicon and metagenomic analyses on Acropora muricata and Galaxea astreata to investigate the diversity and functionality of viruses in healthy and bleached corals. Analysis showed that the alpha diversity of holobionts (bacteria, eukaryotes, zooxanthellae, and lysogenic and lytic viruses) was higher in bleached corals than that in healthy corals. Meanwhile, bleached corals exhibited a relatively higher abundance of specific viral classes, including Revtraviricetes, Arfiviricetes, Faserviricetes, Caudoviricetes, Herviviricetes, and Tectiliviricetes; moreover, we found that the expression levels of functional genes involved in carbon and sulfur metabolism were enriched. An increase in Vibrio abundance has been reported as a notable factor in coral bleaching; our analysis also revealed an increased abundance of Vibrio in bleached coral. Finally, bleached corals contained a higher abundance of Vibrio phages and encoded more virulence factor genes to increase the competitiveness of Vibrio after coral bleaching. In conclusion, we attempted to understand the causes of coral bleaching from the perspective of phage–bacteria–coral tripartite interaction.IMPORTANCEViruses, especially bacteriophages, outnumber other microorganisms by approximately 10-fold and represent the most abundant members of coral holobionts. Corals represent a model system for the study of symbiosis, the influence of viruses on organisms inhabiting healthy coral reef, the role of rapid horizontal gene transfer, and the expression of auxiliary metabolic genes. However, the least studied component of coral holobiont are viruses. Therefore, there is a critical need to investigate the viral community of viruses, and their functionality, in healthy and bleached coral. Here, we compared the composition and functionality of viruses in healthy and bleached corals and found that viruses may participate in the induction of coral bleaching by enhancing the expression of virulence genes and other auxiliary metabolic functions.
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spelling doaj-art-87946b1b61c74d228026ae54c16ad65a2024-12-19T14:00:32ZengAmerican Society for MicrobiologymSphere2379-50422024-12-0191210.1128/msphere.00816-24Changes in the diversity and functionality of viruses that can bleach healthy coralZhengyi Zhang0Mengmeng Tong1Wei Ding2Shuikai Liu3Mui-Choo Jong4Ahmed A. Radwan5Zhonghua Cai6Jin Zhou7Shenzhen Public Platform for Screening and Application of Marine Microbial Resources, Institute for Ocean Engineering, Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong Province, ChinaOcean College, Zhejiang University, Zhoushan, Zhejiang, ChinaShenzhen Zhihai Ocean Biotechnology Co., Ltd., Shenzhen, Guangdong Province, ChinaShenzhen Zhihai Ocean Biotechnology Co., Ltd., Shenzhen, Guangdong Province, ChinaInstitute of Environment and Ecology, Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong, ChinaGenetics and Cytology Department, National Research Centre (NRC), Cairo, EgyptShenzhen Public Platform for Screening and Application of Marine Microbial Resources, Institute for Ocean Engineering, Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong Province, ChinaShenzhen Public Platform for Screening and Application of Marine Microbial Resources, Institute for Ocean Engineering, Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong Province, ChinaABSTRACT Coral microbiomes play a crucial role in maintaining the health and functionality of holobionts. Disruption in the equilibrium of holobionts, including bacteria, fungi, and archaea, can result in the bleaching of coral. However, little is known about the viruses that can infect holobionts in coral, especially bacteriophages. Here, we employed a combination of amplicon and metagenomic analyses on Acropora muricata and Galaxea astreata to investigate the diversity and functionality of viruses in healthy and bleached corals. Analysis showed that the alpha diversity of holobionts (bacteria, eukaryotes, zooxanthellae, and lysogenic and lytic viruses) was higher in bleached corals than that in healthy corals. Meanwhile, bleached corals exhibited a relatively higher abundance of specific viral classes, including Revtraviricetes, Arfiviricetes, Faserviricetes, Caudoviricetes, Herviviricetes, and Tectiliviricetes; moreover, we found that the expression levels of functional genes involved in carbon and sulfur metabolism were enriched. An increase in Vibrio abundance has been reported as a notable factor in coral bleaching; our analysis also revealed an increased abundance of Vibrio in bleached coral. Finally, bleached corals contained a higher abundance of Vibrio phages and encoded more virulence factor genes to increase the competitiveness of Vibrio after coral bleaching. In conclusion, we attempted to understand the causes of coral bleaching from the perspective of phage–bacteria–coral tripartite interaction.IMPORTANCEViruses, especially bacteriophages, outnumber other microorganisms by approximately 10-fold and represent the most abundant members of coral holobionts. Corals represent a model system for the study of symbiosis, the influence of viruses on organisms inhabiting healthy coral reef, the role of rapid horizontal gene transfer, and the expression of auxiliary metabolic genes. However, the least studied component of coral holobiont are viruses. Therefore, there is a critical need to investigate the viral community of viruses, and their functionality, in healthy and bleached coral. Here, we compared the composition and functionality of viruses in healthy and bleached corals and found that viruses may participate in the induction of coral bleaching by enhancing the expression of virulence genes and other auxiliary metabolic functions.https://journals.asm.org/doi/10.1128/msphere.00816-24coral microbiomescoral bleachingvirusesVibrio phages
spellingShingle Zhengyi Zhang
Mengmeng Tong
Wei Ding
Shuikai Liu
Mui-Choo Jong
Ahmed A. Radwan
Zhonghua Cai
Jin Zhou
Changes in the diversity and functionality of viruses that can bleach healthy coral
mSphere
coral microbiomes
coral bleaching
viruses
Vibrio phages
title Changes in the diversity and functionality of viruses that can bleach healthy coral
title_full Changes in the diversity and functionality of viruses that can bleach healthy coral
title_fullStr Changes in the diversity and functionality of viruses that can bleach healthy coral
title_full_unstemmed Changes in the diversity and functionality of viruses that can bleach healthy coral
title_short Changes in the diversity and functionality of viruses that can bleach healthy coral
title_sort changes in the diversity and functionality of viruses that can bleach healthy coral
topic coral microbiomes
coral bleaching
viruses
Vibrio phages
url https://journals.asm.org/doi/10.1128/msphere.00816-24
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