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

Ocean warming, disease, and pollution 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 coral Acropora 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-responsive A. cervicornis parasite, and provide a glimpse at the mechanism of induced disease susceptibility while implicating nutrient exposure in its horizontal transmission. SignificanceThe coral disease crisis has contributed to global declines in coral abundance and diversity and is exacerbated by environmental stressors like eutrophication. Thus, identifying factors that influence coral disease resistance and resilience is a top priority. The Rickettsiales-like bacterium, Candidatus Aquarickettsia rohweri is ubiquitous coral symbiont that is strongly linked to coral disease susceptibility in staghorn coral, and is undergoing positive selection across the Caribbean. Although Ca. A. rohweri is a putative parasite, little is known about the activity of this bacterium in coral tissue. This work supports the role of Ca. A. rohweri as a highly active, nutrient-responsive parasite and proposes a mechanism for how Ca. A. rohweri contributes to coral disease susceptibility, parasite expansion, and horizontal transmission.