A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef‐building corals

Abstract

Nutritional interactions between corals and symbiotic dinoflagellate algae lie at the heart of the structural foundation of coral reefs. Whilst the genetic diversity of Symbiodinium has attracted particular interest because of its contribution to the sensitivity of corals to environmental changes and bleaching (i.e. disruption of coral-dinoflagellate symbiosis), very little is known about the in hospite metabolic capabilities of different Symbiodinium types. Using a combination of stable isotopic labelling and nanoscale secondary ion mass spectrometry (NanoSIMS), we investigated the ability of the intact symbiosis between the reef-building coral Isopora palifera, and Symbiodinium C or D types, to assimilate dissolved inorganic carbon (via photosynthesis) and nitrogen (as ammonium). Our results indicate that Symbiodinium types from two clades naturally associated with I. palifera possess different metabolic capabilities. The Symbiodinium C type fixed and passed significantly more carbon and nitrogen to its coral host than the D type. This study provides further insights into the metabolic plasticity among different Symbiodinium types in hospite and strengthens the evidence that the more temperature-tolerant Symbiodinium D type may be less metabolically beneficial for its coral host under non-stressful conditions.

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

“…Instead, P. verrucosa exhibited strong clade fidelity concomitant with an increase in clade A Symbiodinium . Hence, clade A symbionts seem to perform better in high nitrogen environments when compared to symbionts from clade D. In this regard, it is interesting to note that clade D Symbiodinium exhibited an inferior capacity for nitrogen acquisition compared to other clades at ambient temperatures in previous work (Baker, Andras, Jordán‐Garza, & Fogel, 2013; Pernice et al., 2015). …”

Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora

“…Support for this is provided by recent work that used NanoSIMS to demonstrate ammonium assimilation from 15 N-labelled ammonium ( 15 NH 4 Cl) in cells of both the coral host (that is, Acropora aspera and Isopora palifera) and Symbiodinium symbionts after just 1-h incubation (Pernice et al, 2012;Pernice et al, 2014). NanoSIMS technology has also been used to show the incorporation and translocation of labelled ammonium ( 15 NH 4 ) originating from nitrogen-enriched cultured bacteria (Vibrio sp.…”

Light microenvironment and single-cell gradients of carbon fixation in tissues of symbiont-bearing corals

“…After microsensor measurements, corals were incubated with 13 C-bicarbonate (Supplementary Text S1). NanoSIMS imaging was then applied on coral tissue sections, as described by Pernice et al (2014) to quantify the assimilation of dissolved inorganic carbon into individual Symbiodinium cells across polyp (oral and aboral) and coenosarc tissues of corals. Briefly, corals were incubated in small aquaria with 2 mM NaH 13 CO 3 in artificial sea water (recipe adapted from Harrison et al, 1980).…”

“…Briefly, corals were incubated in small aquaria with 2 mM NaH 13 CO 3 in artificial sea water (recipe adapted from Harrison et al, 1980). After 24 h of isotopic incubation, coral fragments were sampled, chemically fixed and processed for NanoSIMS analyses (see Kopp et al, 2013;Pernice et al, 2012Pernice et al, , 2014 and Supplementary Text S1, Supplementary Figure S1). …”

“…Although such enhanced efficiency under low light often reflects the adaptation of the photosynthetic apparatus (for example, an increase in lightharvesting complexes (Walters, 2005) and reduced cell respiration (Givnish, 1988), it might additionally be the result of physiologically distinct populations or clades of Symbiodinium. Several studies have revealed remarkable genetic and physiological diversities among different Symbiodinium clades (Loram et al, 2007;Stat et al, 2008;Baker et al, 2013;Pernice et al, 2014). Although Favites sp.…”