2023bioRxiv (Cold Spring Harbor Laboratory)Open access

Shifts in the coral microbiome in response to in situ experimental deoxygenation

Rachel D. Howard, Monica D. Schul, Lucia M. Rodriguez Bravo, Andrew H. Altieri, Julie L. Meyer

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Abstract

ABSTRACT Global climate change impacts ocean communities through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, little is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their relative tolerance to hypoxia. We conducted in situ oxygen manipulations on a coral reef in Bahía Almirante, Panama, which has previously experienced episodes of low dissolved oxygen concentrations. Naïve coral colonies (previously unexposed to hypoxia) of massive starlet coral ( Siderastrea siderea ) and Lamarck’s sheet coral ( Agaricia lamarcki ) were transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor. Importance Marine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Deoxygenation on coral reefs will worsen with ongoing climate change, acidification, and eutrophication. We do not yet understand the response of the coral microbiome to hypoxia, and whether this reaction may have a beneficial or harmful role in the coral holobiont. To understand how the coral microbial community structure responds during hypoxic stress, we experimentally lowered the oxygen levels around corals in the field to observe changes in the composition of the coral microbiome. We documented the increase of anaerobic and pathogenic bacteria in the microbiomes of the massive starlet coral ( Siderastrea siderea ) and Lamarck’s sheet coral ( Agaricia lamarcki ) in 48 hours. This work provides fundamental knowledge of the microbial response in the coral holobiont during hypoxia and may provide insight to holobiont function during stress.

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ABSTRACT Global climate change impacts ocean communities through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, little is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their relative tolerance to hypoxia. We conducted in situ oxygen manipulations on a coral reef in Bahía Almirante, Panama, which has previously experienced episodes of low dissolved oxygen concentrations. Naïve coral colonies (previously unexposed to hypoxia) of massive starlet coral ( Siderastrea siderea ) and Lamarck’s sheet coral ( Agaricia lamarcki ) were transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor. Importance Marine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Deoxygenation on coral reefs will worsen with ongoing climate change, acidification, and eutrophication. We do not yet understand the response of the coral microbiome to hypoxia, and whether this reaction may have a beneficial or harmful role in the coral holobiont. To understand how the coral microbial community structure responds during hypoxic stress, we experimentally lowered the oxygen levels around corals in the field to observe changes in the composition of the coral microbiome. We documented the increase of anaerobic and pathogenic bacteria in the microbiomes of the massive starlet coral ( Siderastrea siderea ) and Lamarck’s sheet coral ( Agaricia lamarcki ) in 48 hours. This work provides fundamental knowledge of the microbial response in the coral holobiont during hypoxia and may provide insight to holobiont function during stress.

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Available abstract

ABSTRACT Global climate change impacts ocean communities through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, little is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their relative tolerance to hypoxia. We conducted in situ oxygen manipulations on a coral reef in Bahía Almirante, Panama, which has previously experienced episodes of low dissolved oxygen concentrations. Naïve coral colonies (previously unexposed to hypoxia) of massive starlet coral ( Siderastrea siderea ) and Lamarck’s sheet coral ( Agaricia lamarcki ) were transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor. Importance Marine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Deoxygenation on coral reefs will worsen with ongoing climate change, acidification, and eutrophication. We do not yet understand the response of the coral microbiome to hypoxia, and whether this reaction may have a beneficial or harmful role in the coral holobiont. To understand how the coral microbial community structure responds during hypoxic stress, we experimentally lowered the oxygen levels around corals in the field to observe changes in the composition of the coral microbiome. We documented the increase of anaerobic and pathogenic bacteria in the microbiomes of the massive starlet coral ( Siderastrea siderea ) and Lamarck’s sheet coral ( Agaricia lamarcki ) in 48 hours. This work provides fundamental knowledge of the microbial response in the coral holobiont during hypoxia and may provide insight to holobiont function during stress.

Key concepts: Holobiont, Coral, Microbiome, Biology, Hypoxia (environmental), Ecology, Anthozoa, Coral reef

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