Long-Term Temperature Stress in the Coral Model Aiptasia Supports the "Anna Karenina Principle" for Bacterial Microbiomes

Abstract

The understanding of host-microbial partnerships has become a hot topic during the last decade as it has been shown that associated microbiota play critical roles in the host physiological functions and susceptibility to diseases. Moreover, the microbiome may contribute to host resilience to environmental stressors. The sea anemone Aiptasia is a good laboratory model system to study corals and their microbial symbiosis. In this regard, studying its bacterial microbiota provides a better understanding of cnidarian metaorganisms as a whole. Here, we investigated the bacterial communities of different Aiptasia host-symbiont combinations under long-term heat stress in laboratory conditions. Following a 16S rRNA gene sequencing approach we were able to detect significant differences in the bacterial composition and structure of Aiptasia reared at different temperatures. A higher number of taxa (i.e., species richness), and consequently increased α-diversity and β-dispersion, were observed in the microbiomes of heat-stressed individuals across all host strains and experimental batches. Our findings are in line with the recently proposed Anna Karenina principle (AKP) for animal microbiomes, which states that dysbiotic or stressed organisms have a more variable and unstable microbiome than healthy ones. Microbial interactions affect the fitness and survival of their hosts, thus exploring the AKP effect on animal microbiomes is important to understand host resilience. Our data contributes to the current knowledge of the Aiptasia holobiont and to the growing field of study of host-associated microbiomes.

Keywords: 16S rRNA gene; dispersion; microbiome; temperature; β-diversity.

FIGURE 1

Bacterial community composition of different Aiptasia host-symbiont combinations on the family level (Greengenes database, bootstrap ≥ 60). Each color represents one taxon across all samples. Less abundant taxa <1%), comprising 199 distinct families are grouped under “others.” Pie charts display the average composition of anemones at 25°C (left) and 32°C (right). Sample labels indicate Aiptasia group, batch (i.e., tank) and replicate, respectively (e.g., CC7_r1.1).

FIGURE 2

Overview of α-diversity measurements for different Aiptasia host-symbiont combinations. Number of observed OTUs (A), Chao1 richness estimator (B), Inverse Simpson (C), and Simpson’s evenness (D) indexes. Each boxplot shows six data points corresponding to the replicate samples of each host-symbiont combination. Different shades of blue and red represent 25°C and 32°C temperatures, respectively.

FIGURE 3

Differentially abundant OTUs (agglomerated by family) in Aiptasia between temperatures. Log2 fold change values indicate OTUs that show significant differential abundance in anemones reared at 32°C compared to those from 25°C (p < 0.05). Taxonomic annotation shown is based on BLASTn closest hit.

FIGURE 4

Principal coordinate analysis based on unweigthed Unifrac distances showing changes in the bacterial community composition of Aiptasia across temperatures. Different shades of blue and red show 25°C and 32°C, respectively. Ellipses represent 95% confidence intervals. Percentages on axes indicate the variation explained by the two coordinates.