The engine of the reef: photobiology of the coral-algal symbiosis

Abstract

Coral reef ecosystems thrive in tropical oligotrophic oceans because of the relationship between corals and endosymbiotic dinoflagellate algae called Symbiodinium. Symbiodinium convert sunlight and carbon dioxide into organic carbon and oxygen to fuel coral growth and calcification, creating habitat for these diverse and productive ecosystems. Light is thus a key regulating factor shaping the productivity, physiology, and ecology of the coral holobiont. Similar to all oxygenic photoautotrophs, Symbiodinium must safely harvest sunlight for photosynthesis and dissipate excess energy to prevent oxidative stress. Oxidative stress is caused by environmental stressors such as those associated with global climate change, and ultimately leads to breakdown of the coral-algal symbiosis known as coral bleaching. Recently, large-scale coral bleaching events have become pervasive and frequent threatening and endangering coral reefs. Because the coral-algal symbiosis is the biological engine producing the reef, the future of coral reef ecosystems depends on the ecophysiology of the symbiosis. This review examines the photobiology of the coral-algal symbiosis with particular focus on the photophysiological responses and timescales of corals and Symbiodinium. Additionally, this review summarizes the light environment and its dynamics, the vulnerability of the symbiosis to oxidative stress, the abiotic and biotic factors influencing photosynthesis, the diversity of the coral-algal symbiosis, and recent advances in the field. Studies integrating physiology with the developing "omics" fields will provide new insights into the coral-algal symbiosis. Greater physiological and ecological understanding of the coral-algal symbiosis is needed for protection and conservation of coral reefs.

Keywords: Symbiodinium; acclimation; dinoflagellate; ecophysiology; photophysiology; photoprotection; scleractinian corals.

FIGURE 1

“An oasis in a desert ocean”: coral reef seascapes powered by the coral–algal symbiosis. (A) Aerial view of coral reef architecture in shallow, oligotrophic tropical waters of Fiji.(B) Reef-building corals create habitats for vibrant communities boasting incredible biodiversity and productivity. This photograph was taken in the heart of the Coral Triangle in Raja Ampat, Indonesia. (C) Corals are colonial invertebrates, made up of genetically identical individual polyps connected by living tissue (coenosarc). The coral golden hue of Seriatopora hystrix comes from symbiotic dinoflagellates located within their cells. Scale bar represents 1 cm. (D) The biological engine of the reef – endosymbiotic dinoflagellates of the genus Symbiodinium in coral cells: fluorescence microscopy image showing a Montipora capitata coral egg (green fluorescence from coral fluorescent proteins) and intracellular Symbiodinium (red fluorescence from chlorophyll). Symbiodinium provides photosynthetic products and oxygen to fuel coral growth and calcification. Scale bar represents 50 μm. (Images by M. S. Roth.)

FIGURE 2

Schematic of the light environment of the coral–algal symbiosis. (A) Irradiance rapidly declines with depth in the ocean. (B) Light spectrum narrows with depth, becoming primarily blue. Wavelength attenuation properties and absorption by inorganic and organic matter in the water column determine the spectral composition at depth. (C) Fundamental light dynamics in the coral–algal symbiosis. (1) The principal light is downwelling incident sunlight. If the incident light is not absorbed by the coral or Symbiodinium, it is (2) primarily reflected by the coral skeleton as diffuse reflectance, and (3) secondarily enters the porous skeleton and then re-emerges elsewhere as diffuse reflectance. The multiple scattering by the skeleton causes the light to pass back through the coral tissue, amplifying the light Symbiodinium is exposed to. Symbiodinium is located within a host vacuole called the symbiosome (Inspired by Enríquez et al., 2005; Kirk, 2010; Marcelino et al., 2013).

FIGURE 3

Pathways of light energy utilization by Symbiodinium. The funnel scheme of the photosynthetic apparatus depicts the possible fates of absorbed light. When sunlight is absorbed by chlorophyll, the singlet-state excitation of chlorophyll (¹Chl*) is formed and the excitation energy can be (1) used to drive photochemistry, (2) re-emitted as fluorescence, (3) dissipated as heat (NPQ), or (4) decayed via the chlorophyll triplet state (³Chl*), which produces reactive oxygen species as a by-product. Multiple types of reactive oxygen species are produced during photosynthetic electron flow. When the light exceeds what can be processed through these pathways, there is a high potential for the accumulation of reactive oxygen species and ultimately oxidative stress (inspired by Müller et al., 2001 and Demmig-Adams and Adams, 2002).