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Nitrate enrichment has lineage specific effects on Pocillopora acuta adults, but no transgenerational effects in planulae

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Abstract

Local-scale nutrient pollution can alter coral growth and reproductive output, as well as their resident communities of microorganisms (dinoflagellates in the family Symbiodiniaceae, bacteria). Yet, the ways in which nutrient pollution alters coral interactions with their microorganisms are not fully understood, and no studies have tested for transgenerational impacts of nutrient stress on coral holobionts. To investigate this, colonies of Pocillopora acuta were enriched with nitrate in situ for up to one year and monitored for planulation. Gene expression, resident microbial communities and holobiont traits were characterized in adults, as well as in planulae. Although separated by > 5 m, clonality and chimerism were observed in the majority of coral colonies. Lineage- and treatment-specific effects of nitrate treatment were detected in adults and planulae. Nitrate-enriched adults contained higher densities of Symbiodiniaceae and exhibited downregulation of genes involved in the synthesis of nitrogenous compounds. Planulae harbored higher Symbiodiniaceae and bacteria diversity than adults; this study constitutes the first assessment of these microorganisms from individual planulae. Coral-associated bacteria communities were Endozoicomonas-dominated and were not altered by nutrient treatment. Planula-associated bacteria communities differed from their parents but not from parental exposure to nutrients, and no changes in fecundity or settlement success resulted from enrichment. Taken together, these findings suggest that adult corals acclimate to chronic nutrient pollution by harboring higher Symbiodiniaceae densities, with no observed negative effects on the subsequent generation.

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Data availability

Raw gene expression and microbial data are archived as an NCBI SRA via bioproject PRJNA694169. Holobiont data and R code for microbial analysis are available at https://github.com/LaurenHK/Pacu_nitrate_Moorea_microbe.git. R code for tag-seq analysis is available at https://github.com/mariestrader/Pacu_nitrate_Moorea.git.

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Acknowledgements

We thank Anna Knochel, Hailee Clover, and Jake Emmert (Moody Gardens Aquarium) for field support and Olivia Simon for laboratory support. The Alabama Super Computer Authority provided computational resources. A Lewis and Clark Grant from the American Philosophical Society to LHK, a John E. Parish Fellowship from Wiess College and a Clara Carter Higgins Scholarship from the Garden Club of America to JAS, and a NSF Graduate Research Fellowship to KES supported this project. This project was also supported by the US National Science Foundation (OCE #1935308 to MES, OCE #1547952 to DEB, and OCE #1635798 to AMSC), an Early-Career Research Fellowship (#2000009651 to AMSC) from the Gulf Research Program of the National Academies of Sciences, and start-up funds to AMSC from Rice University. Samples were collected under research permit https://doi.org/10.21973/N3R94R. Research was completed under permits issued by the Territorial Government of French Polynesia (Délégation à la Recherche) and the Haut-Commissariat de la République en Polynésie Francaise (DTRT) (Protocole d’Accueil 2013–2019), and we thank the Délégation à la Recherche and DTRT for their continued support.

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  1. Marie E. Strader and Lauren I. Howe-Kerr have contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Sciences, Auburn University, Auburn, AL, USA

    Marie E. Strader

  2. BioSciences at Rice, Rice University, Houston, TX, USA

    Lauren I. Howe-Kerr, Jordan A. Sims, Amanda N. Shore & Adrienne M. S. Correa

  3. Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, CA, USA

    Kelly E. Speare & Deron E. Burkepile

  4. Department of Biology, Farmingdale State College, New York, NY, USA

    Amanda N. Shore

  5. Department of Environmental Science and Policy, George Mason University, Fairfax, VA, USA

    Jordan A. Sims

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  1. Marie E. Strader
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Correspondence to Marie E. Strader.

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Strader, M.E., Howe-Kerr, L.I., Sims, J.A. et al. Nitrate enrichment has lineage specific effects on Pocillopora acuta adults, but no transgenerational effects in planulae. Coral Reefs 41, 303–317 (2022). https://doi.org/10.1007/s00338-022-02236-9

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