Novel Adaptive Photosynthetic Characteristics of Mesophotic Symbiotic Microalgae within the Reef-Building Coral, Stylophora pistillata

Abstract

Photosynthetic coral reef structures extend from the shallow sundrenched waters to the dimly lit, "twilight" mesophotic depths. For their resident endosymbiotic dinoflagellates, primarily from the genus Symbiodinium spp., this represents a photic environment that varies ∼15-fold in intensity and also differs in spectral composition. We examined photosynthesis in the scleractinian coral Stylophora pistillata in shallow (3 m) and mesophotic settings (65 m) in the northern Red Sea. Symbiodinium spp. in corals originating from the mesophotic environment consistently performed below their photosynthetic compensation point and also exhibited distinct light harvesting antenna organization. In addition, the non-photochemical quenching activity of Symbiodinium spp. from mesophotic corals was shown to be considerably lower than those found in shallow corals, showing they have fewer defenses to high-light settings. Over a period of almost 4 years, we extensively utilized closed circuit Trimix rebreather diving to perform the study. Phylogenetic analysis showed that shallow corals (3 m) transplanted to a deep reef environment (65 m) maintained their initial Symbiodinium spp. community (clade A), rather than taking on deep low-light clades (clade C), demonstrating that shallow S. pistillata acclimate to low-light mesophotic environments while maintaining their shallow photosynthetic traits. Mesophotic corals exhibited static depth-related chlorophyll content per cell, a decrease in PSI activity and enhanced sigmoidal fluorescence rise kinetics. The sigmoidal fluorescence rise kinetics we observed in mesophotic corals is an indication of energy transfer between photosynthetic units. We postulate that at mesophotic depths, a community of adapted Symbiodinium spp. utilize a unique adaptation to lower light conditions by shifting their light harvesting to a PSII based system, where PSII is structured near PSI, with additional PCP soluble Einbinder et al.Novel Photosynthetic Characteristics of Mesophotic Photosymbionts antenna also trapping light that is funneled to the PSI reaction center. In this study, we provide evidence that mesophotic Symbiodinium spp. have developed novel adaptive low-light characteristics consisting of a cooperative system for excitation energy transfer between photosynthetic units that maximizes light utilization.

Coral Morphology Portrays the Spatial Distribution and Population Size-Structure Along a 5–100 m Depth Gradient

“…For shallow reefs, the coral contribution is largely due to fast-growing corals, such as branching and corymbose, which are common coral morphologies in many shallow-water reefs; whereas at the mesophotic depths the coral contribution may result from a combination of high environmental stability and slow-growing morphologies, which are considered to be more tolerant to stressful environments (Darling et al, 2012), consequently allowing coral populations to achieve balanced and stable size-populations. Moreover, corals in low-light environments (e.g., mesophotic) maximize their surface area at the colony morphological level, thus maximizing their light reception (Hughes and Jackson, 1985;Lesser et al, 2010;Einbinder et al, 2016). Consequently, encrusting, laminar, and massive morphologies are better fitted to survive and flourish under such extreme optical conditions, although some branching and digitate depth-generalist species are known to adjust their morphology (i.e., becoming flatter) with depth (Eyal et al, 2015(Eyal et al, , 2019Einbinder et al, 2016;Kahng et al, 2019).…”

Effects of depth on reef fish communities: Insights of a “deep refuge hypothesis” from Southwestern Atlantic reefs

“…Regarding photo-physiological traits, recent findings [ 15 , 16 ] show increased chlorophyll concentrations in coral holobionts occurring in mesophotic depths. Increased concentrations in antenna pigments per photosynthetic units (PSU) have been related to an acclimation mechanism to low-light regimes [ 71 ]. In the present study, as well as in previous works [ 45 , 71 ], no evidences of acclimation mechanisms ( e .…”

“…Increased concentrations in antenna pigments per photosynthetic units (PSU) have been related to an acclimation mechanism to low-light regimes [ 71 ]. In the present study, as well as in previous works [ 45 , 71 ], no evidences of acclimation mechanisms ( e . g .…”

Membrane Inlet Mass Spectrometry: A Powerful Tool for Algal Research

“…The involvement of Flavodiiron proteins (Flvs) in light-dependent O 2 uptake was further established in cyanobacteria (Helman et al, 2003;Allahverdiyeva et al, 2013), and more recently in microalgae (Chaux et al, 2017). MIMS is nowadays widely used to understand the fate of the photosynthetic electron flow in various environmental conditions and mutant of cyanobacteria (Ermakova et al, 2016;Boatman et al, 2018;Luimstra et al, 2019), microalgae (Fisher and Halsey, 2016), or coral reef symbiosis (Einbinder et al, 2016).…”