Metabolic interactions between algal symbionts and invertebrate hosts

Abstract

Some invertebrates have enlisted autotrophic unicellular algae to provide a competitive metabolic advantage in nutritionally demanding habitats. These symbioses exist primarily but not exclusively in shallow tropical oceanic waters where clear water and low nutrient levels provide maximal advantage to the association. Mostly, the endosymbiotic algae are localized in host cells surrounded by a host-derived membrane (symbiosome). This anatomy has required adaptation of the host biochemistry to allow transport of the normally excreted inorganic nutrients (CO2, NH3 and PO4 3-) to the alga. In return, the symbiont supplies photosynthetic products to the host to meet its energy demands. Most attention has focused on the metabolism of CO2 and nitrogen sources. Carbon-concentrating mechanisms are a feature of all algae, but the products exported to the host following photosynthetic CO2 fixation vary. Identification of the stimulus for release of algal photosynthate in hospite remains elusive. Nitrogen assimilation within the symbiosis is an essential element in the host's control over the alga. Recent studies have concentrated on cnidarians because of the impact of global climate change resulting in coral bleaching. The loss of the algal symbiont and its metabolic contribution to the host has the potential to result in the transition from a coral-dominated to an algal-dominated ecosystem.

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

“…It is possible then that the coral host maintains this concentration gradient in the areas surrounding symbiotic dinoflagellates by rapidly fixing ammonium into amino acids, which can be used by the coral or transferred to the algal cells later on. This hypothesis has been somehow neglected so far (but see : Miller and Yellowlees, 1989;Wang and Douglas, 1998;Yellowlees et al, 2008) based on evidence that GS/GOGAT cycle, the fastest route for incorporating ammonium into amino acids through glutamate, is not widespread in animals. However, recent studies demonstrated that GS/GOGAT cycle is active in several metazoans (Scaraffia et al, 2005;Hansen and Moran, 2011) and our analyses using BLAST algorithm (Altschul et al, 1990) indicate that transcripts encoding proteins with high similarities to the domains of GOGAT are present in two cnidarian genomes (Nematostella vectensis (Sullivan et al, 2006), genBank accession number: XP_001630774.1; Acropora digitifera (Shinzato et al, 2011), http://marinegenomics.oist.jp/acropora _digitifera/, gene ID: aug_v2a.08445.t1; Supplementary Table S2).…”

“…Together, the coral and their dinoflagellate partners are able to acquire inorganic nitrogen, which is advantageous in an environment where planktonic supply may be episodic (Yellowlees et al, 2008;Sheppard et al, 2009). Among the different dissolved nutrients, ammonium is the preferred source of nitrogen for symbiotic corals ( Figure 1a) (Grover et al, 2002(Grover et al, , 2008.…”

“…Both the coral host and the algae possess the enzymatic machinery required to incorporate ammonium into their tissues. It has been proposed that the majority of ammonium is assimilated either by the dinoflagellate symbiont via the glutamine synthetase/ glutamine:2-oxoglutarate aminotransferase (GS/ GOGAT) cycle (D'Elia et al, 1983;Roberts et al, 1999Roberts et al, , 2001 or by the coral host via the action of GS and/or glutamate dehydrogenase (Figure 1c) (Miller and Yellowlees, 1989;Wang and Douglas, 1998;Yellowlees et al, 2008).…”

“…Metabolic studies on coral-dinoflagellate symbioses generally involve the unnatural culture of both symbiotic partners separately or the separation of algal and host tissue fractions, an experimental procedure, which is often incomplete and hampered by crosscontamination (Yellowlees et al, 2008). In this context, recent advances in a high-resolution isotopic imaging technology, the sub-micrometer scale ion microprobe technique referred to as NanoSIMS provides direct imaging and quantification of the metabolic exchanges within an intact symbiosis following stable isotope labeling (Lechene et al, 2006(Lechene et al, , 2007Kuypers, 2007;Musat et al, 2008;Dattagupta et al, 2009;Foster et al, 2011).…”

Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia)

“…Heterotrophy contributes most to the material needs (nitrogen compounds), while photoautotrophy contributes to the energy and carbon demand of the coral (Anthony and Fabricius 2000;Piniak et al 2003;Houlbrèque and Ferrier-Pagès 2008). The intense recycling and exchange of nutrients between the coral animal and the zooxanthellae make corals particularly adapted to life in nutrient-limited waters (Muscatine and Porter 1977;Furla et al 2005;Yellowlees et al 2008).…”