Microbiome signatures in Acropora cervicornis are associated with genotypic resistance to elevated nutrients and heat stress

Abstract

The staghorn coral, Acropora cervicornis, was once abundant in the Caribbean, but now is listed as critically endangered. To recover A. cervicornis populations, restoration efforts have focused on preserving genetic diversity and increasing coral cover. However, identifying stress-resistant corals can help to increase restoration success, by allocating genotypes to reefs where they are more likely to survive. We assessed the performance (growth, survivorship, and photochemical efficiency) and characterized the microbiome (prokaryotes) of six A. cervicornis genotypes that were maintained at control temperatures (~ 26 °C) and either ambient nutrients or elevated nutrients (elevated NH4, and elevated NH4 + PO4) for > 2 months. We then compared how these parameters changed when the corals were exposed to heat stress (3 weeks at ~ 31.5 °C). We found that exposure to elevated nutrients reduced A. cervicornis performance under control temperatures and heat stress. However, there was a wide range of variation among genotypes, with three genotypes maintaining relatively higher survivorship and growth rates when exposed to nutrients alone, and nutrients followed by heat stress. Heat stress alone changed the microbial composition among genotypes more than elevated nutrients alone, but heat stress also interacted with nutrient pre-exposure to affect microbial communities. The relative abundance of Midichloriaceae and Spirochaetaceae varied by coral genotype and a high abundance of these bacterial taxa was a positive predictor of coral survivorship rate, suggesting a microbial signature that could aid in identifying resistant A. cervicornis genotypes. Our findings suggest there is significant variation among genotypes in the response of A. cervicornis to elevated nutrients and temperatures. Resistant genotypes may be identifiable via their microbiomes and prioritized for outplanting at sites that experience nutrient pollution. Large-scale microbiome screening may help expedite targeted outplanting and could be tested and extended to facilitate the identification of genotypes with other resistance characteristics.