Antibiotics Alter Pocillopora Coral-Symbiodiniaceae-Bacteria Interactions and Cause Microbial Dysbiosis During Heat Stress

Michael T Connelly,Pi-Jen Liu,Crystal J Mcrae,Cecily E Martin,Nikki Traylor-Knowles

doi:10.3389/fmars.2021.814124

Abstract

Symbioses between eukaryotes and their associated microbial communities are fundamental processes that affect organisms’ ecology and evolution. A unique example of this is reef-building corals that maintain symbiotic associations with dinoflagellate algae (Symbiodiniaceae) and bacteria that affect coral health through various mechanisms. However, little is understood about how coral-associated bacteria communities affect holobiont heat tolerance. In this study, we investigated these interactions in four Pocillopora coral colonies belonging to three cryptic species by subjecting fragments to treatments with antibiotics intended to suppress the normal bacteria community, followed by acute heat stress. Separate treatments with only antibiotics or heat stress were conducted to compare the effects of individual stressors on holobiont transcriptome responses and microbiome shifts. Across all Pocillopora species examined, combined antibiotics and heat stress treatment significantly altered coral-associated bacteria communities and caused major changes in both coral and Cladocopium algal symbiont gene expression. Individually, heat stress impaired Pocillopora protein translation and activated DNA repair processes, while antibiotics treatments caused downregulation of Pocillopora amino acid and inorganic ion transport and metabolism genes and Cladocopium photosynthesis genes. Combined antibiotics-heat stress treatments caused synergistic effects on Pocillopora and Cladocopium gene expression including enhanced expression of oxidative stress response genes, programed cell death pathways and proteolytic enzymes that indicate an exacerbated response to heat stress following bacteria community suppression. Collectively, these results provide further evidence that corals and their Symbiodiniaceae and bacteria communities engage in highly coordinated metabolic interactions that are crucial for coral holobiont health, homeostasis, and heat tolerance.

Highlights

Microbial symbioses are fundamental to the structure and functioning of marine ecosystems, and influence marine organisms’ ecology, evolution, and stress responses (O’Brien et al, 2019; Wilkins et al, 2019; Apprill, 2020)
Antibiotics are increasingly being considered for use in coral disease intervention strategies and as environmental pollutants that are potentially damaging to coral health (Zhang R. et al, 2018; Zhang R. et al, 2019; Neely et al, 2020; Walker et al, 2021)
Our experiment reveals that antibiotic suppression of coral-associated bacteria communities produces dramatic changes in Pocillopora coral and Cladocopium symbiont gene expression and bacteria community composition, resulting in microbial dysbiosis and diminished holobiont heat tolerance

Summary

Introduction

Microbial symbioses are fundamental to the structure and functioning of marine ecosystems, and influence marine organisms’ ecology, evolution, and stress responses (O’Brien et al, 2019; Wilkins et al, 2019; Apprill, 2020). Certain coral-associated bacteria have been investigated for their roles in affecting corals’ responses to heat stress, with different bacteria taxa exerting either negative or positive effects on coral holobiont resistance and resilience (Tout et al, 2015; Zaneveld et al, 2016; Ziegler et al, 2017, 2019; Epstein et al, 2019; Avila-Magaña et al, 2021) Other environmental stressors such as nutrient enrichment can alter coral bacteria communities (Pogoreutz et al, 2018; Ziegler et al, 2019), but the interactive effects of different stressors applied in combination and their effects on coral health are still the focus of much research (Maher et al, 2019)

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Conclusion