Microbiomes of a disease-resistant genotype of Acropora cervicornis are resistant to acute, but not chronic, nutrient enrichment

Abstract

Chronically high levels of inorganic nutrients have been documented in Florida’s coral reefs and are linked to increased prevalence and severity of coral bleaching and disease. Naturally disease-resistant genotypes of the staghorn coral Acropora cervicornis are rare, and it is unknown whether prolonged exposure to acute or chronic high nutrient levels will reduce the disease tolerance of these genotypes. Recently, the relative abundance of the bacterial genus Aquarickettsia was identified as a significant indicator of disease susceptibility in A. cervicornis, and the abundance of this bacterial species was previously found to increase under chronic and acute nutrient enrichment. We therefore examined the impact of common constituents of nutrient pollution (phosphate, nitrate, and ammonium) on microbial community structure in a disease-resistant genotype with naturally low abundances of Aquarickettsia. We found that although this putative parasite responded positively to nutrient enrichment in a disease-resistant host, relative abundances remained low (< 0.5%). Further, while microbial diversity was not altered significantly after 3 weeks of nutrient enrichment, 6 weeks of enrichment was sufficient to shift microbiome diversity and composition. Coral growth rates were also reduced by 6 weeks of nitrate treatment compared to untreated conditions. Together these data suggest that the microbiomes of disease-resistant A. cervicornis may be initially resistant to shifts in microbial community structure, but succumb to compositional and diversity alterations after more sustained environmental pressure. As the maintenance of disease-resistant genotypes is critical for coral population management and restoration, a complete understanding of how these genotypes respond to environmental stressors is necessary to predict their longevity.

Nutrient enrichment alters gene expression in ‘Ca.’Aquarickettsia rohweri, promoting parasite expansion and horizontal transmission

“…To test the impacts of nutrient enrichment on A. cervicornis health and microbiome community function, a six-week tank experiment was conducted as previously described (24,27) at the Mote Marine Laboratory International Center for Coral Reef Research & Restoration (24°39'41.9"N, 81°27'15.5"W) in Summerland Key, Florida from April to June 2019. The experiment was conducted in 4.7 L flow-through, temperature-controlled aquaria with natural locally-sourced sea water from the Atlantic side of the Keys.…”

“…A. rohweri specific marker gene) revealed that 'Ca.' A. rohweri responded positively to nutrient enrichment in both host genotypes, however it remained at low relative abundances in the disease-resistant genotype, ML-7 (<0.5% of the total bacterial community) (24). In the disease-susceptible genotype, M-50, 'Ca.'…”

“…A. rohweri (89.7%), while 'Ca.' A. rohweri makes up a minor constituent of disease resistant microbiomes (2.5%) (18,19,24). Further, 'Ca.'…”

“…Recently, we performed a manipulative tank experiment to disentangle the individual and combined impacts of eutrophication on 'Ca.' A. rohweri abundance within A. cervicornis microbiomes (24,27). We exposed a disease susceptible A. cervicornis genotype (ML-50) and a disease resistant A. cervicornis genotype (ML-7), to elevated levels of nitrate, ammonium, phosphate, or a combination of the three for six weeks and evaluated microbiome composition and host fitness.…”