Multiple stressors interact primarily through antagonism to drive changes in the coral microbiome

Abstract

Perturbations in natural systems generally are the combination of multiple interactions among individual stressors. However, methods to interpret the effects of interacting stressors remain challenging and are biased to identifying synergies which are prioritized in conservation. Therefore we conducted a multiple stressor experiment (no stress, single, double, triple) on the coral Pocillopora meandrina to evaluate how its microbiome changes compositionally with increasing levels of perturbation. We found that effects of nutrient enrichment, simulated predation, and increased temperature are antagonistic, rather than synergistic or additive, for a variety of microbial community diversity measures. Importantly, high temperature and scarring alone had the greatest effect on changing microbial community composition and diversity. Using differential abundance analysis, we found that the main effects of stressors increased the abundance of opportunistic taxa, and two-way interactions among stressors acted antagonistically on this increase, while three-way interactions acted synergistically. These data suggest that: (1) multiple statistical analyses should be conducted for a complete assessment of microbial community dynamics, (2) for some statistical metrics multiple stressors do not necessarily increase the disruption of microbiomes over single stressors in this coral species, and (3) the observed stressor-induced community dysbiosis is characterized by a proliferation of opportunists rather than a depletion of a proposed coral symbiont of the genus Endozoicomonas .

Parrotfish predation drives distinct microbial communities in reef-building corals

“…Increased microbiome variability is consistent with previous studies showing that numerous animals, including corals, exhibit elevated community variability when exposed to stressors (i.e. the Anna Karenina Principle [64];), such as mechanical wounding [39]. This further indicates the potential for parrotfish to increase dysbiosis susceptibility in corals via corallivory.…”

“…In addition, microbiomes of predated corals were characterized by moderate abundance (59.9% at T f ) of the putative beneficial symbiont Hahellaceae at 48 h when compared to Ti (83.9%). Lower abundance of Hahellaceae bacterial taxa is a pattern previously reported in stressed, mechanical injured, and predated corals [9,38,39,41].…”

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

“…Similarly, bacterial members of the coral holobiont are sensitive to changing environmental conditions but have been evaluated less extensively under increasing seawater temperatures. Research on bacterial community dynamics under temperature stress demonstrates shifts to more disease-associated states, increases in community variability, compromised function of beneficial microbiota, and selection for potentially pathogenic bacteria (Ritchie, 2006;Bourne et al, 2008;Thurber et al, 2009;Mouchka et al, 2010;Maher et al, 2019). Given that coral microbiota are thought to play an important role in nutrient cycling and antimicrobial protection (Ritchie, 2006;Wegley et al, 2007), it is important to understand how their response to thermal stress events can mitigate or exacerbate host survival and ecosystem resilience.…”

“…While the effects of excess nitrogen levels on coral physiology have been well-documented, less is known about their potential to alter coral-associated bacterial communities, especially when combined with stressors such as ocean warming. For corals maintained in aquaria, both nitrate and ammonium were sufficient to destabilize the coral-associated bacterial community, although ammonium-treated corals remained more similar compositionally to controls than nitrate-treated corals (Maher et al, 2019;Rice et al, 2019). In the Florida Keys, nitrogen and phosphorous enrichment made corals more susceptible to mortality from predation, above-average seawater temperatures, and bacterial opportunism (Zaneveld et al, 2016).…”

“…In sharp contrast to the Florida Keys which remain in a state of low total coral cover, the fore reef of Mo'orea, French Polynesia, has recovered from numerous landscape-scale perturbations within about a decade with total coral cover reaching ∼50% in 2019 (Adjeroud et al, 2002(Adjeroud et al, , 2009Berumen and Pratchett, 2006;Penin et al, 2007;Adam et al, 2011Adam et al, , 2014Trapon et al, 2011;Holbrook et al, 2018). Mesocosm experiments on Pocillopora meandrina microbiomes in Mo'orea showed that while nutrients and the interaction between nutrient enrichment and high temperature had an effect on individual members of the microbiome, temperature alone had the strongest effect on alpha and beta diversity overall (Maher et al, 2019). However, the temperature stress applied in the experiment was not sufficient to induce bleaching or mortality (Rice et al, 2019).…”