Long-term coral microbial community acclimatization is associated with coral survival in a changing climate

Abstract

The plasticity of some coral-associated microbial communities under stressors like warming and ocean acidification suggests the microbiome has a role in the acclimatization of corals to future ocean conditions. Here, we evaluated the acclimatization potential of coral-associated microbial communities of four Hawaiian coral species (Porites compressa, Porites lobata, Montipora capitata, and Pocillopora acuta) over 22-month mesocosm experiment. The corals were exposed to one of four treatments: control, ocean acidification, ocean warming, or combined future ocean conditions. Over the 22-month study, 33-67% of corals died or experienced a loss of most live tissue coverage in the ocean warming and future ocean treatments while only 0-10% died in the ocean acidification and control. Among the survivors, coral-associated microbial communities responded to the chronic future ocean treatment in one of two ways: (1) microbial communities differed between the control and future ocean treatment, suggesting the potential capacity for acclimatization, or (2) microbial communities did not significantly differ between the control and future ocean treatment. The first strategy was observed in both Porites species and was associated with higher survivorship compared to M. capitata and P. acuta which exhibited the second strategy. Interestingly, the microbial community responses to chronic stressors were independent of coral physiology. These findings indicate acclimatization of microbial communities may confer resilience in some species of corals to chronic warming associated with climate change. However, M. capitata genets that survived the future ocean treatment hosted significantly different microbial communities from those that died, suggesting the microbial communities of the survivors conferred some resilience. Thus, even among coral species with inflexible microbial communities, some individuals may already be tolerant to future ocean conditions. These findings suggest that coral-associated microbial communities could play an important role in the persistence of some corals and underlie climate change-driven shifts in coral community composition.

Fig 1. Diagram showing how coral-associated microbial communities were compared within and among treatments, using the future ocean treatment as an example.

(A) To evaluate if the microbial community composition changed in response to the future ocean treatment, comparisons were restricted to genets that survived and were able to be sampled in both the control and the future ocean treatment. (B) To evaluate if the baseline microbial community composition differed among genets based on survival in future ocean treatment, comparisons were restricted to genets in the control whose lineages had greater than 30% live tissue coverage (shown in black squares) or less than 30% live tissue coverage (shown in red squares) following 22 months in the future ocean treatment.

Fig 2. Percent survivorship based on 30% live tissue threshold for each coral species in each treatment at the end of the 22-month mesocosm experiment.

Fig 3. Microbial communities associated with corals in the control.

(A) NMDS plot of microbial communities associated with each coral species in the control. Each species significantly differed from the other (See S2a Table in S1 File for PERMANOVA statistical details). (B) Mean Relative abundances of the most common microbial Orders associated with each coral species in the control. Only Orders with a relative abundance greater than 2.0% in at least one coral species are represented individually.

Fig 4. NMDS plots of coral-associated microbial community composition between the control (closed circles) and the future ocean treatments (open circles) for genets of each coral species that survived the future ocean treatment (Illustrated in Fig 1A).

Significant differences detected by PERMANOVA analyses (p < 0.05) are indicated in the top left corner (NS = no significant difference) with corresponding statistical details in S7 Table in S1 File. Comparison of microbial community composition by Order between the control and future ocean treatments for each coral species is in S3 Fig.

Fig 5. NMDS plots of coral-associated microbial community composition of A) Porites compressa, B) Porites lobata, C) Montipora capitata, and D) Pocillopora acuta in the control categorized by greater than 30% live tissue coverage (closed circles) or less than 30% live tissue coverage (X) of their genetic counterparts in the future ocean treatment (Illustrated in Fig 1B).

Significant differences detected by PERMANOVA analyses (p < 0.05) are indicated in the top left corner (NS = no significant difference) with corresponding statistical details in S11 Table in S1 File.