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

   https://doi.org/10.1038/s41598-023-30615-x  

   Klinges, J. Grace ; Patel, Shalvi H. ; Duke, William C. ; Muller, Erinn M. ; Vega Thurber, Rebecca L. ( March 2023 , Scientific Reports)

   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 coralAcropora cervicornisare 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 genusAquarickettsiawas identified as a significant indicator of disease susceptibility inA. 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 ofAquarickettsia.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-resistantA. cervicornismay be initially resistant to shifts in microbial community structure,more »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.

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2. A phenomic modeling approach for using chlorophyll-a fluorescence-based measurements on coral photosymbionts

   https://doi.org/10.3389/fmars.2023.1092202  

   Hoadley, Kenneth D. ; Lockridge, Grant ; McQuagge, Audrey ; Pahl, K. Blue ; Lowry, Sean ; Wong, Sophie ; Craig, Zachary ; Petrik, Chelsea ; Klepac, Courtney ; Muller, Erinn M. ( March 2023 , Frontiers in Marine Science)

   We test a newly developed instrument prototype which utilizes time-resolved chlorophyll- a fluorescence techniques and fluctuating light to characterize Symbiodiniaceae functional traits across seven different coral species under cultivation as part of ongoing restoration efforts in the Florida Keys. While traditional chlorophyll- a fluorescence techniques only provide a handful of algal biometrics, the system and protocol we have developed generates > 1000 dynamic measurements in a short (~11 min) time frame. Resulting ‘high-content’ algal biometric data revealed distinct phenotypes, which broadly corresponded to genus-level Symbiodiniaceae designations determined using quantitative PCR. Next, algal biometric data from Acropora cervicornis (10 genotypes) and A. palmata (5 genotypes) coral fragments was correlated with bleaching response metrics collected after a two month-long exposure to high temperature. A network analysis identified 1973 correlations (Spearman R > 0.5) between algal biometrics and various bleaching response metrics. These identified biomarkers of thermal stress were then utilized to train a predictive model, and when tested against the same A. cervicornis and A. palmata coral fragments, yielded high correlation (R = 0.92) with measured thermal response (reductions in absorbance by chlorophyll-a). When applied to all seven coral species, the model ranked fragments dominated by Cladocopium or Breviolum symbionts as moremore »bleaching susceptible than corals harboring thermally tolerant symbionts ( Durusdinium ). While direct testing of bleaching predictions on novel genotypes is still needed, our device and modeling pipeline may help broaden the scalability of existing approaches for determining thermal tolerance in reef corals. Our instrument prototype and analytical pipeline aligns with recent coral restoration assessments that call for the development of novel tools for improving scalability of coral restoration programs.« less
3. The coral symbiont Candidatus Aquarickettsia is variably abundant in threatened Caribbean acroporids and transmitted horizontally

   https://doi.org/10.1038/s41396-021-01077-8  

   Baker, Lydia J. ; Reich, Hannah G. ; Kitchen, Sheila A. ; Grace Klinges, J. ; Koch, Hanna R. ; Baums, Iliana B. ; Muller, Erinn M. ; Thurber, Rebecca Vega ( August 2021 , The ISME Journal)

   The symbiont “CandidatusAquarickettsia rohweri” infects a diversity of aquatic hosts. In the threatened Caribbean coral,Acropora cervicornis,Aquarickettsiaproliferates in response to increased nutrient exposure, resulting in suppressed growth and increased disease susceptibility and mortality of coral. This study evaluated the extent, as well as the ecology and evolution ofAquarickettsiainfecting threatened corals,Ac. cervicornis, andAc. palmataand their hybrid (“Ac. prolifera”).Aquarickettsiawas found in all acroporids, with coral host and geographic location impacting the infection magnitude. Phylogenomic and genome-wide single-nucleotide variant analysis ofAquarickettsiafound phylogenetic clustering by geographic region, not by coral taxon. Analysis ofAquarickettsiafixation indices suggests multiple sequential infections of the same coral colony are unlikely. Furthermore, relative to other Rickettsiales species,Aquarickettsiais undergoing positive selection, with Florida populations experiencing greater positive selection relative to other Caribbean locations. This may be due in part toAquarickettsiaproliferating in response to greater nutrient stress in Florida, as indicated by greater in situ replication rates in these corals.Aquarickettsiawas not found to significantly codiversify with either the coral animal or the coral’s algal symbiont (Symbiodinium“fitti”). Quantitative PCR analysis showed that gametes, larvae, recruits, and juveniles from susceptible, captive-reared coral genets were not infected withAquarickettsia. Thus, horizontal transmission ofAquarickettsiavia coral mucocytes or an unidentified host is more likely. The prevalence ofAquarickettsiainAc. cervicornisandmore »its high abundance in the Florida coral population suggests that coral disease mitigation efforts focus on preventing early infection via horizontal transmission.

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4. Phosphate enrichment induces increased dominance of the parasite Aquarickettsia in the coral Acropora cervicornis

   https://doi.org/10.1093/femsec/fiac013  

   Klinges, J Grace ; Patel, Shalvi H ; Duke, William C ; Muller, Erinn M ; Vega Thurber, Rebecca L ( February 2022 , FEMS Microbiology Ecology)

   Abstract Nutrient pollution is linked to coral disease susceptibility and severity, but the mechanism behind this effect remains underexplored. A recently identified bacterial species, ‘Ca. Aquarickettsia rohweri,’ is hypothesized to parasitize the Caribbean staghorn coral, Acropora cervicornis, leading to reduced coral growth and increased disease susceptibility. Aquarickettsia rohweri is hypothesized to assimilate host metabolites and ATP and was previously demonstrated to be highly nutrient-responsive. As nutrient enrichment is a pervasive issue in the Caribbean, this study examined the effects of common nutrient pollutants (nitrate, ammonium, and phosphate) on a disease-susceptible genotype of A. cervicornis. Microbial diversity was found to decline over the course of the experiment in phosphate-, nitrate-, and combined-treated samples, and quantitative PCR indicated that Aquarickettsia abundance increased significantly across all treatments. Only treatments amended with phosphate, however, exhibited a significant shift in Aquarickettsia abundance relative to other taxa. Furthermore, corals exposed to phosphate had significantly lower linear extension than untreated or nitrate-treated corals after 3 weeks of nutrient exposure. Together these data suggest that while experimental tank conditions, with an elevated nutrient regime associated with coastal waters, increased total bacterial abundance, only the addition of phosphate significantly altered the ratios of Aquarickettsia compared to other members ofmore »the microbiome.« less
5. Genetic differences in thermal tolerance among colonies of threatened coral Acropora cervicornis: potential for adaptation to increasing temperature

   https://doi.org/10.3354/meps13407  

   Yetsko, K ; Ross, M ; Bellantuono, A ; Merselis, D ; Rodriquez-Lanetty, M ; Gilg, MR ( July 2020 , Marine Ecology Progress Series)

   Climate change is resulting in warmer temperatures that are negatively impacting corals. Understanding how much individuals within a population vary in their thermal tolerance and whether this variation is heritable is important in determining whether a species can adapt to climate change. To address this, Acropora cervicornis fragments from 20 genetically distinct colonies collected from the Coral Restoration Foundation Tavernier nursery (Florida, USA) were kept at either ambient (28 ± 1°C) or elevated (32 ± 1°C) temperatures, and mortality was monitored for 26 d. Both broad-sense ( H 2 ) and narrow-sense ( h 2 ) heritability of thermal tolerance were estimated to determine the amount of genetic variation underlying survival to elevated temperature. To understand the physiological basis of thermal tolerance, tissue from both treatments was taken 12 h after the start of the experiment to investigate gene expression at the mRNA and protein level between tolerant and susceptible colonies. Results revealed that this population has considerable total genetic variation in thermal tolerance ( H 2 = 0.528), but low variance in relatedness among colonies prevented us from making any conclusions regarding h 2 . Despite high transcriptomic variability among and within colonies, 40 genes were consistently and significantlymore »different between tolerant and susceptible colonies, and could be potential biomarkers for thermal tolerance should they be verified in a larger sample. Overall, the results suggest that this population has substantial genetic variation for traits that directly impact thermal tolerance; however, their response to projected increases in temperature will depend on more precise estimates of the additive components of this variation ( h 2 ).« less