A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera

Abstract

Light underpins the health and function of coral reef ecosystems, where symbiotic partnerships with photosynthetic algae constitute the life support system of the reef. Decades of research have given us detailed knowledge of the photoprotective capacity of phototrophic organisms, yet little is known about the role of the host in providing photoprotection in symbiotic systems. Here we show that the intracellular symbionts within the large photosymbiotic foraminifera Marginopora vertebralis exhibit phototactic behaviour, and that the phototactic movement of the symbionts is accomplished by the host, through rapid actin-mediated relocation of the symbionts deeper into the cavities within the calcium carbonate test. Using a photosynthetic inhibitor, we identified that the infochemical signalling for host regulation is photosynthetically derived, highlighting the presence of an intimate communication between the symbiont and the host. Our results emphasise the central importance of the host in photosymbiotic photoprotection via a new mechanism in foraminifera that can serve as a platform for exploring host-symbiont communication in other photosymbiotic organisms.

Figure 1

Change in photophysiology and reflectance under different irradiance treatments over time. (a) Effective quantum yield of PSII (ΔF/F_M') for the surface (circles) and underside (triangles) of Marginopora vertebralis exposed to constant light (CL; black) and increasing light (IL; blue) over 3 h (200, 400 and 800 μmol photons m⁻² s⁻¹) with a final hour of recovery (130 μmol photons m⁻² s⁻¹) (n=8). (b) Excitation pressure over PSII (Q_M) on the surface of M. vertebralis (circles; n=8) and the de-epoxidation ratio of photoprotective pigments (bars; n=3) exposed to constant low (130 μmol photons m⁻² s⁻¹) light (black) and increasing irradiance over 3 h+recovery (blue). (c) Relative change in average pixel intensity on the surface (circles) and underside (triangles) of M. vertebralis exposed to constant (black) and increasing light over 3 h+recovery (blue) (n=5–8). (d) Spectral reflectance as a percentage of a pure white standard measured on the surface of M. vertebralis exposed to increasing irradiances. Arrows indicate characteristic absorption wavelengths of Symbiodinium: chlorophyll a (435–440, 675 nm), chlorophyll c (460 nm) and peridinin (480–490 nm), dashed lines indicate s.e.m. (n=8). (e) Total integrated reflectance at the surface of M. vertebralis exposed to increasing irradiances over time (T0–T3) (n=8). (f) Photographs illustrating the sequential whitening (from top left to bottom right) of one M. vertebralis exposed to high light. Scale bar=5 mm. Data represent mean±s.e.m. Asterisk (*) indicates values that are significantly different between light treatments and superscript letters denote significantly different over time (P<0.05). A full colour version of this figure is available at the ISME journal online.

Figure 2

Tissue sections illustrating the localisation of the symbionts within the test of Marginopora vertebralis exposed to 130, 400 and 800 μmol photons m⁻² s⁻¹. (a) Complete tissue section of an M. vertebralis tests, scale bar=200 μm, (b) close up of three different tissue sections from foraminifera exposed to different light intensities (indicated in the picture), scale bar=50 μm. Green is the auto-fluorescence of the animal tissue and red is the symbiont chlorophyll. A full colour version of this figure is available at the ISME journal online.

Figure 3

Change in photosynthetic efficiency and pixel intensity in the presence of the actin inhibitor cytochalasin B. (a) Effective quantum yield of PSII (ΔF/F_M') at constant (CL; black) and increasing (IL; blue) light intensities in the presence (cyto; circles) and absence (DMSO; triangles) of cytochalasin B. Insert shows the ΔF/F_M' at 800 μmol photons m⁻² s⁻¹ as a percentage of the initial values. (b) Relative change in pixel intensity at constant (black) and increasing light (blue) intensities in the presence (circles) and absence (triangles) of cytochalasin B. Data represent mean±s.e.m., n=6–8. Asterisk (*) indicates values that are significantly different between light treatments and superscript letters denote significantly different over time (P<0.05). A full colour version of this figure is available at the ISME journal online.

Figure 4

Change in symbiont motility in the presence of cytochalasin B. (a) Symbiodinium (red) within individual chambers of Marginopora vertebralis test (green), (b) average speed of movement of Symbiodinium within chambers incubated with 0, 10 and 20 μg ml⁻¹ of cytochalasin B, respectively, as a percent of control (data were square root transformed; n=18). Scale bar=25 μm. Data represent mean±s.e.m. Superscript letters denote significant difference between treatments (P<0.05). A full colour version of this figure is available at the ISME journal online.

Figure 5

Symbiont photosynthesis and vertical migration in the presence of DCMU. Relative change in pixel intensity (bars) and effective quantum yield of PSII (diamonds) in Marginopora vertebralis exposed to 130 μmol photons m⁻² s⁻¹ (black bars) and 800 μmol photons m⁻² s⁻¹ (blue bars) in the presence of DMSO (control) or DCMU (n=6–8). Error bars on ΔF/F_M' are smaller than the symbol. Data represent the mean±s.e.m. Superscript letters denote significant difference between treatments (P<0.05). A full colour version of this figure is available at the ISME journal online.