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

Abstract

Ocean warming, disease, and pollution have contributed to global declines in coral abundances and diversity. In the Caribbean, corals previously dominated reefs, providing an architectural framework for diverse ecological habitats, but have significantly declined due to infectious microbial disease. Key species like coralAcropora cervicornis, are now considered critically endangered, prompting researchers to focus on scientific endeavors to identify factors that influence coral disease resistance and resilience. We previously showed that disease susceptibility, growth rates, and bleaching risk were all associated with the abundance of a single bacterial parasite,′Ca.′Aquarickettsia rohweri which proliferates in vivo under nutrient enrichment. Yet how nutrients influence parasite physiology and life history strategies within its host are unknown. We performed microscopy and transcriptomic analyses of′Ca.′A. rohweri populations during a 6–week nutrient exposure experiment. Microscopy showed that this parasite was abundant in coral tissue and densely packed in mucocytes prior to nutrient enrichment.′Ca.′A. rohweri energy scavenging genes and those potentially involved in this habitat transition are significantly upregulated during enrichment. Specifically, transcripts involved in signaling, virulence, two-component systems, and nutrient import genes are elevated under higher nutrients. These data support the predicted role of′Ca.′A. rohweri as a highly active nutrient-responsiveA. cervicornisparasite, and provide a glimpse at the mechanism of induced disease susceptibility while implicating nutrient exposure in its horizontal transmission.