Coral Microbiomes Demonstrate Flexibility and Resilience Through a Reduction in Community Diversity Following a Thermal Stress Event

Abstract

Thermal stress increases community diversity, community variability, and the abundance of potentially pathogenic microbial taxa in the coral microbiome. Nutrient pollution, such as excess nitrogen can also interact with thermal stress to exacerbate host fitness degradation. However, it is unclear how different forms of nitrogen (nitrate vs. ammonium/urea) interact with bleaching-level temperature stress to drive changes in coral microbiomes, especially on reefs with histories of resilience. We used a 13-month field experiment spanning a thermal stress event in the Austral summer of 2016 on the oligotrophic fore reef of Mo'orea, French Polynesia to test how different forms of nitrogen (nitrate vs. urea) impact the resistance and resilience of coral microbiomes. For Acropora, Pocillopora, and Porites corals, we found no significant differences in diversity metrics between control, nitrate-, and urea-treated corals during thermal stress. In fact, thermal stress may have overwhelmed any effects of nitrogen. Although all three coral hosts were dominated by the bacterial clade Endozoicomonas which is a proposed beneficial coral symbiont, each host differed through time in patterns of community diversity and variability. These differences between hosts may reflect different strategies for restructuring or maintaining microbiome composition to cope with environmental stress. Contrary to our expectation, post-stress microbiomes did not return to prestress community composition, but rather were less diverse and increasingly dominated by Endozoicomonas. The dominance of Endozoicomonas in microbiomes 10 months after peak sea surface temperatures may suggest its ability to utilize host metabolic products of thermal stress for a sustained competitive advantage against other microbial members. If Endozoicomonas is a beneficial coral symbiont, its proliferation after warm summer months could provide evidence of its ability to mitigate coral holobiont dysbiosis to thermal stress and of resilience in coral microbiomes.

Thermal Stress Interacts With Surgeonfish Feces to Increase Coral Susceptibility to Dysbiosis and Reduce Tissue Regeneration

“…Interestingly, some of the aforementioned taxa, such as Vibrionaceae, Colwelliaceae, Clostridiaceae, Arcobacteraceae and Desulfobulbaceae, are often associated with stressed corals, diseased lesions or bleaching ( Thompson et al, 2006 ; Weil et al, 2006 ; Sunagawa et al, 2009 ; Arotsker et al, 2015 ). Additionally, microbiomes of corals exposed to feces showed a significant decrease in the relative abundance of the potential beneficial symbiont Endozoicomonadaceae between T0 and T24 (from 71.65% to 27.3%) - an observation that aligns well with previous results on stressed corals ( Morrow et al, 2015 ; Glasl et al, 2016 ; Ziegler et al, 2017 ; Pootakham et al, 2019 ; Maher et al, 2020 ).…”

“…The recovery of coral microbiomes was associated with a considerable increase in the relative abundance of Endozoicomonadaceae in microbiomes of corals exposed to feces at the end of the experiment (TF) compared to T48 (from 38.6% to 67.2%). Our findings parallel with a previous study demonstrating the resilience of Endozoicomonadaceae in corals following stressful conditions (Maher et al, 2020).…”

The coral symbiontCandidatusAquarickettsia is variably abundant in threatened Caribbean acroporids and transmitted horizontally

“…Differential exposure to these stressors may result in dissimilar disease resistance by location, with higher occurrences of disease resistance in Florida (27%) relative to similar populations found in Panama (6%) and USVI (8%) [39]. This in turn may influence the prevalence of infection of the nutrient-stress responsive A. rohweri [6,40]. Although disentangling the impact of host and environment will require further sampling and experimental efforts, our comparative analysis of A. rohweri populations provides insight into how infection of this symbiont may be influenced by environmental conditions.…”

Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals

“…However, changes in coral microbiome observed richness over time and treatment ( Figure 2 A) also indicates that coral microbiomes may be resilient to nutrient enrichment, as richness levels between treatments became more similar by T3, which would be the end of the nutrient pulse, and stay similar till the last time point (T4). We previously saw similar patterns in coral microbiomes after exposure to a natural temperature anomaly in which species richness peaked after peak temperatures, and declined following a recovery period [ 54 ].…”

“…Next, the V4 region of the 16S rRNA gene was amplified via 2-step PCR coupling forward and reverse primers 515F (5′-GTG YCA GCM GCC GCG GTA A-3′) [ 52 ] and 806R (5′-GGA CTA CNV GGG TWT CTA AT-3′) [ 53 ]. First-step PCR was conducted according to the reaction and thermocycler protocol described in Maher et al 2020 [ 54 ]. Second-step PCR was conducted according to the methods described in Ezzat et al 2021 [ 26 ].…”