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

  • Host Microbe Interactions
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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.

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Acknowledgments

We thank Young Duk Koh for collecting samples and Tae Young Jang, An Suk Lim, and Éric Potvin for technical support. This paper was supported by the National Research Foundation of Korea Grant funded by the Korea Government/MSIP (NRF-2015-M1A5A1041806) and Management of marine organisms causing ecological disturbance and harmful effect Program of Korea Institute of Marine Science and Technology Promotion (KIMST) award to HJJ. Contributions provided by T.C.L. were funded in part by the Pennsylvania State University and a grant from the National Science Foundation (IOS-1258058).

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Correspondence to Hae Jin Jeong or Todd C LaJeunesse.

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Figure S1

The correspondence between estimated cell densities based on qPCR fluorescence measurements and hemocytometer counts. (GIF 107 kb)

High resolution image (EPS 649 kb)

Figure S2

Positive relationship between cell densities of B2* and S. voratum graphed by water temperatures at the time samples when collected. Pairwise comparisons where considered only when concentrations of B2* occurred above of 50,000 cells/gww, a range where qPCR estimates of cell numbers are more accurate. (GIF 131 kb)

High resolution image (EPS 947 kb)

Figure S3

Correspondence between estimated cell concentrations of S. voratum (per gram wet weight of host tissue) and its prevalence (percentage) in polyps of A. japonica. (GIF 81 kb)

High resolution image (EPS 655 kb)

Figure S4

Concentration of ammonium (NH4), nitrate (NO3), phosphate (PO4), and silica dioxide (SiO2) in surface waters at Jeju Island, Korea every month over the 15-month survey period. These values are graphed against (A) measures of Chlorophyll a content, as well as the prevalence (percent) of (B) Symbiodinium sp. Clade B, and (C) S. voratum (Clade E) detected in the polyps (n = 90) of Alveopora japonica using qPCR. (GIF 123 kb)

High resolution image (EPS 1040 kb)

Table S1

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Table S2

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Table S3

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Lee, M.J., Jeong, H.J., Jang, S.H. et al. Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals. Microb Ecol 71, 771–783 (2016). https://doi.org/10.1007/s00248-015-0724-2

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