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.

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

“…This approach holds a dual premise: firstly, intragenomic allelic diversity of the ITS2 marker allows to resolve differences within and between individuals and species previously not possible (Batovska et al, 2016); secondly, in the case of Symbiodinium, deep sequencing of ITS2 diversity may uncover symbiont associations previously not detected (Arif et al, 2014;Boulotte et al, 2016). However, the contribution of low abundant Symbiodinium taxa to host resilience remains to be determined (Lee et al, 2016).…”

Rapid adaptive responses to climate change in corals

“…The generally greater diversity of Symbiodinium communities in early life-history stages compared to in adults 79 could be viewed as a bet-hedging strategy, providing juvenile corals with the opportunity to fine-tune endosymbiotic communities to suit ambient conditions. Finally, the retention of low-abundance background Symbiodinium types in adult stages of some corals 16,81 may provide further adaptive capacity to the holobiont (but see 82), facilitating future shuffling of dominant Symbiodinium types in response to changing environmental conditions 76,83 .…”

“…The short generation time of Symbiodinium means that its rate of mutation is much faster than for the coral host 18 , and this, combined with its large within-host population sizes, potentially facilitates rapid responses to altered thermal environments, either through selection of existing genetic variants or through the evolution of novel adaptations 73,74 . Alternatively, the composition of host-associated Symbiodinium communities may vary temporally in response to environmental conditions or at different host lifehistory stages 75 , either through shuffling of existing symbionts 76 or through acquisition of new Symbiodinium types from the environment (that is, switching) 16 . In particular, high genetic and phenotypic diversity among Symbiodinium taxa provides scope for some coral species to vary the composition of associated Symbiodinium communities, balancing photosynthetic activity (and hence growth) with stress tolerance, a type of acclimatory mechanism for responding to environmental extremes 76,77,78 .…”

“…Moreover, exact mechanisms and the extent to which they have an effect are still unclear and under discussion 15 . Understanding multigenerational effects in corals is further complicated by the intimate relationships that they form with diverse suites of microorganisms that may contribute to phenotypic plasticity 16,17 PERSPECTIVE NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE3374…”

Short-Term Thermal Acclimation Modifies the Metabolic Condition of the Coral Holobiont

“…Reefs that have been subjected to frequent thermal anomalies and/or highly variable thermal regimes over the past century tend to exhibit higher bleaching thresholds than those exposed to stable conditions suggesting a certain degree of plasticity exists in the coral holobionts' thermal resistance (Carilli et al, 2012). Indeed, some coral species exhibit increased energy reserves (Rodrigues and Grottoli, 2007;Grottoli et al, 2014) and/or changes in the dominant Symbiodinium type after bleaching events (Howells et al, 2012;Boulotte et al, 2016), while others modify their microbial community . A recent analysis of temperature fluctuations recorded over 27 years on the Great Barrier Reef, Australia, found that 75% of all thermal stress events were characterized by temperatures greater than the maximum monthly mean temperature (MMM) but less than the bleaching threshold (MMM+1-2 • C).…”