Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals

Abstract

Speculation surrounds the importance of ecologically cryptic Symbiodinium spp. (dinoflagellates) that occur at low abundances in reef-building corals and in the surrounding environment. Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to deduce the ecology and functional significance of these populations and whether they might contribute to the response of coral-dinoflagellate mutualisms to climate change. Quantitative PCR was used here to diagnose the prevalence, seasonal variation, and abundances of Symbiodinium spp. within and between colonies of the coral, Alveopora japonica. Consistent with broader geographic sampling, only one species comprised 99.9 %, or greater, the population of symbionts in every sample. However, other Symbiodinium including the non-mutualistic species, Symbiodinium voratum, were often detected, but at estimated cell densities thousands-fold less than the dominant symbiont. The temporal variation in prevalence and abundances of these "background" Symbiodinium could not be definitively related to any particular environmental factor including seasonality and water chemistry. The prevalence (proportion detected among host samples), but not abundance, of S. voratum may weakly correspond to increases in environmental inorganic silica (SiO2) and possibly nitrogen (NO3). When multiple background Symbiodinium occurred within an individual polyp, the average cell densities were positively correlated, suggesting non-specific processes of cell sorting and retention by the animal. While these findings substantiate the existence of a broader, yet uncharacterized, diversity of Symbiodinium, we conclude that only those species which can occur in high abundance and are temporally stable are ultimately important to coral-dinoflagellate mutualisms. Many transient Symbiodinium spp., which occur only at trace abundances in the coral's microbiome, belong to different functional guilds and likely have little, if any, importance to a coral's physiology. The successful integration between host and symbiont into a stable functional unit should therefore be considered when defining host-symbiont specificity.

Rapid adaptive responses to climate change in corals

“…Thus the emergent property of adaptive capacity of the holobiont could simply reflect 'selfish' evolution on the part of the symbiont. However, not all 'symbionts' are beneficial, for example, some Symbiodinium types are almost certainly opportunists that provide little or no benefit to their coral hosts 82,101 ; a number of bacteria are pathogenic, causing a variety of diseases in corals 102 ; and coral-associated bacteria may become pathogenic through the acquisition of prophages 103 . It is also conceivable that proviruses associated with bacteria or Symbiodinium could cause host-cell lysis upon emergence from the lysogenic state triggered by environmental stress.…”

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). Regardless of these considerations, the highest species diversity is found within clade C, that dominates IndoPacific coral reefs and is also one of the most abundant clades in the Atlantic (LaJeunesse, 2005).…”

Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata

“…Consequently, the physiological implications of such shifts are only beginning to be explored. Whilst some background symbionts appear to have no functional role [70], recent network analyses of 46 coral genera provide evidence of the importance of cryptic Symbiodinium communities, in which rare symbionts appear to significantly contribute to symbiosis stability [71]. Similarly, the rare bacterial biosphere is important to holobiont physiology for a range of both plant and animal symbioses [29] and may act to acclimatize the holobiont to new conditions, as postulated for corals [11,72].…”