Decline of a distinct coral reef holobiont community under ocean acidification
Abstract Background Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet mo...
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| Format: | Article |
| Language: | English |
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BMC
2024-04-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01683-y |
| _version_ | 1797199352532303872 |
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| author | Jake Williams Nathalie Pettorelli Aaron C. Hartmann Robert A. Quinn Laetitia Plaisance Michael O’Mahoney Chris P. Meyer Katharina E. Fabricius Nancy Knowlton Emma Ransome |
| author_facet | Jake Williams Nathalie Pettorelli Aaron C. Hartmann Robert A. Quinn Laetitia Plaisance Michael O’Mahoney Chris P. Meyer Katharina E. Fabricius Nancy Knowlton Emma Ransome |
| author_sort | Jake Williams |
| collection | DOAJ |
| description | Abstract Background Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH — an important global coral reef stressor — can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. Results We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. Conclusions We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem change. Video Abstract |
| first_indexed | 2024-04-24T07:14:23Z |
| format | Article |
| id | doaj.art-b0025b456b9d42d790b97067ba274239 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-24T07:14:23Z |
| publishDate | 2024-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-b0025b456b9d42d790b97067ba2742392024-04-21T11:24:57ZengBMCMicrobiome2049-26182024-04-0112111610.1186/s40168-023-01683-yDecline of a distinct coral reef holobiont community under ocean acidificationJake Williams0Nathalie Pettorelli1Aaron C. Hartmann2Robert A. Quinn3Laetitia Plaisance4Michael O’Mahoney5Chris P. Meyer6Katharina E. Fabricius7Nancy Knowlton8Emma Ransome9Georgina Mace Centre for the Living Planet, Department of Life Sciences, Imperial College LondonInstitute of Zoology, Zoological Society of LondonDepartment of Organismic and Evolutionary Biology, Harvard UniversityDepartment of Biochemistry and Molecular Biology, Michigan State UniversityLaboratoire Evolution Et Diversité Biologique, CNRS/UPSNational Museum of Natural History, Smithsonian InstitutionNational Museum of Natural History, Smithsonian InstitutionAustralian Institute of Marine ScienceNational Museum of Natural History, Smithsonian InstitutionGeorgina Mace Centre for the Living Planet, Department of Life Sciences, Imperial College LondonAbstract Background Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH — an important global coral reef stressor — can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. Results We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. Conclusions We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem change. Video Abstracthttps://doi.org/10.1186/s40168-023-01683-yMicrobialisationOcean acidificationMultiomicsHolobiontAutonomous Reef Monitoring StructuresEcosystem collapse |
| spellingShingle | Jake Williams Nathalie Pettorelli Aaron C. Hartmann Robert A. Quinn Laetitia Plaisance Michael O’Mahoney Chris P. Meyer Katharina E. Fabricius Nancy Knowlton Emma Ransome Decline of a distinct coral reef holobiont community under ocean acidification Microbiome Microbialisation Ocean acidification Multiomics Holobiont Autonomous Reef Monitoring Structures Ecosystem collapse |
| title | Decline of a distinct coral reef holobiont community under ocean acidification |
| title_full | Decline of a distinct coral reef holobiont community under ocean acidification |
| title_fullStr | Decline of a distinct coral reef holobiont community under ocean acidification |
| title_full_unstemmed | Decline of a distinct coral reef holobiont community under ocean acidification |
| title_short | Decline of a distinct coral reef holobiont community under ocean acidification |
| title_sort | decline of a distinct coral reef holobiont community under ocean acidification |
| topic | Microbialisation Ocean acidification Multiomics Holobiont Autonomous Reef Monitoring Structures Ecosystem collapse |
| url | https://doi.org/10.1186/s40168-023-01683-y |
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