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Genomic signatures in the coral holobiont reveal host adaptations driven by Holocene climate change and reef specific symbionts.

ABSTRACT: Genetic signatures caused by demographic and adaptive processes during past climatic shifts can inform predictions of species' responses to anthropogenic climate change. To identify these signatures in Acropora tenuis, a reef-building coral threatened by global warming, we first assembled the genome from long reads and then used shallow whole-genome resequencing of 150 colonies from the central inshore Great Barrier Reef to inform population genomic analyses. We identify population structure in the host that reflects a Pleistocene split, whereas photosymbiont differences between reefs most likely reflect contemporary (Holocene) conditions. Signatures of selection in the host were associated with genes linked to diverse processes including osmotic regulation, skeletal development, and the establishment and maintenance of symbiosis. Our results suggest that adaptation to post-glacial climate change in A. tenuis has involved selection on many genes, while differences in symbiont specificity between reefs appear to be unrelated to host population structure.

SUBMITTER: Cooke I

PROVIDER: S-EPMC7695477 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Genomic signatures in the coral holobiont reveal host adaptations driven by Holocene climate change and reef specific symbionts.

Cooke Ira I Ying Hua H Forêt Sylvain S Bongaerts Pim P Strugnell Jan M JM Simakov Oleg O Zhang Jia J Field Matt A MA Rodriguez-Lanetty Mauricio M Bell Sara C SC Bourne David G DG van Oppen Madeleine Jh MJ Ragan Mark A MA Miller David J DJ

Science advances 20201127 48

Genetic signatures caused by demographic and adaptive processes during past climatic shifts can inform predictions of species' responses to anthropogenic climate change. To identify these signatures in <i>Acropora tenuis</i>, a reef-building coral threatened by global warming, we first assembled the genome from long reads and then used shallow whole-genome resequencing of 150 colonies from the central inshore Great Barrier Reef to inform population genomic analyses. We identify population struct ...[more]

PMID: 33246955

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Project description:BackgroundMicrobes 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.ResultsWe 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.ConclusionsWe 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 changed. Video Abstract.

Dataset Information

Genomic signatures in the coral holobiont reveal host adaptations driven by Holocene climate change and reef specific symbionts.

Publications

Genomic signatures in the coral holobiont reveal host adaptations driven by Holocene climate change and reef specific symbionts.

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