Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals

Abstract

Reef-building corals possess a range of acclimatisation and adaptation mechanisms to respond to seawater temperature increases. In some corals, thermal tolerance increases through community composition changes of their dinoflagellate endosymbionts (Symbiodinium spp.), but this mechanism is believed to be limited to the Symbiodinium types already present in the coral tissue acquired during early life stages. Compelling evidence for symbiont switching, that is, the acquisition of novel Symbiodinium types from the environment, by adult coral colonies, is currently lacking. Using deep sequencing analysis of Symbiodinium rDNA internal transcribed spacer 2 (ITS2) PCR amplicons from two pocilloporid coral species, we show evidence consistent with de novo acquisition of Symbiodinium types from the environment by adult corals following two consecutive bleaching events. Most of these newly detected symbionts remained in the rare biosphere (background types occurring below 1% relative abundance), but one novel type reached a relative abundance of ~33%. Two de novo acquired Symbiodinium types belong to the thermally resistant clade D, suggesting that this switching may have been driven by consecutive thermal bleaching events. Our results are particularly important given the maternal mode of Symbiodinium transmission in the study species, which generally results in high symbiont specificity. These findings will cause a paradigm shift in our understanding of coral-Symbiodinium symbiosis flexibility and mechanisms of environmental acclimatisation in corals.

Figure 1

Summary of Symbiodinium diversity in Pocillopora damicornis (a) and Stylophora pistillata (b) from four collection periods spanning May 2010 to September 2012. Pie charts represent the mean relative abundances of Symbiodinium types across all sampled colonies detected at each time point. Types that are dominant at any of the time points are represented in orange, brown or yellow; and types belonging to the rare biosphere throughout the sampling period are represented in grey. Bar graphs represent the abundances (expressed in number of sequencing reads) of Symbiodinium types in the rare biosphere only; and black stars represent a switching event. A switching event was deemed to occur when, during any one sampling a type was detected among multiple samples, but was absent from previous sampling times among any sample. Note that only the most abundant types and the ones that shuffled or switched are shown in this figure. See Supplementary Figures S1 and S2 for the complete figure of all the Symbiodinium background types detected for each period of time.

Figure 2

Non-metric multidimensional scaling ordination (nMDS) representing the Symbiodinium genetic structure from the resemblance matrix of Pocillopora damicornis and Stylophora pistillata centroids belonging to samples collected from 2010 to 2012. The nMDS showed a temporal partitioning within hosts of the Symbiodinium types divided into two distinct groups: May 2010, September 2010 and March 2011 are clustered together while September 2012 is widely separated. This highlights a substantial change in the structure of Symbiodinium assemblage 18 months after the second bleaching event. The bar chart represents the average of Shannon diversity over time within the two Pocilloporidae coral species. Error bars represent 95% confidence interval (Cl).