DMSP biosynthesis by an animal and its role in coral thermal stress response

Abstract

Globally, reef-building corals are the most prolific producers of dimethylsulphoniopropionate (DMSP) 1,2 , a central molecule in the marine sulphur cycle and precursor of the climate-active gas dimethylsulphide 3,4 . At present, DMSP production by corals is attributed entirely to their algal endosymbiont, Symbiodinium 2 . Combining chemical, genomic and molecular approaches, we show that coral juveniles produce DMSP in the absence of algal symbionts. DMSP levels increased up to 54% over time in newly settled coral juveniles lacking algal endosymbionts, and further increases, up to 76%, were recorded when juveniles were subjected to thermal stress. We uncovered coral orthologues of two algal genes recently identified in DMSP biosynthesis, strongly indicating that corals possess the enzymatic machinery necessary for DMSP production. Our results overturn the paradigm that photosynthetic organisms are the sole biological source of DMSP, and highlight the double jeopardy represented by worldwide declining coral cover, as the potential to alleviate thermal stress through coral-produced DMSP declines correspondingly.It is widely accepted that the production of dimethylsulphoniopropionate (DMSP), a central molecule in the marine sulphur cycle, is restricted to marine algae and a few species of intertidal plants 5. Marine bacteria subsequently use DMSP as a source of sulphur and carbon and can metabolize this compound into the volatile gas dimethylsulphide (DMS) 6 , by which the largest natural flux of sulphur enters the atmosphere where it exerts considerable influence on atmospheric chemistry 7 . Despite recent controversy regarding the impact of DMS emissions on global climate 8 , DMS is probably involved in local climate regulation through its oxidation into aerosol particles that induce the formation of clouds and increase their reflectivity, thereby reducing light levels and water temperatures in the marine environment 3,4 . Concentrations of DMSP and DMS found in reef-building corals are among the highest recorded in the environment 1,2 , but it has been assumed that DMSP production derives solely from the coral's endosymbiotic microalgae Symbiodinium. Evidence that the total amounts of DMSP recorded in corals are consistently higher than levels present in Symbiodinium cells alone 9,10 raises the possibility of a cryptic source of DMSP in reef-building corals. A clear understanding of the sources of DMSP on reefs and the possible effects that global warming may have on DMSP production is paramount, given the influence that coralreef-derived sulphur emissions may have on local climates 11 . Corals in the genus Acropora are the most abundant reef-building organisms in the Indo-Pacific region 12 and, as broadcast spawners, they acquire Symbiodinium from their surrounding environment after larval development. The Symbiodinium-free larvae of this genus provide a unique opportunity to investigate Symbiodinium-independent production of DMSP in corals. Results presented here demonstrate that coral hosts (kingdom: Ani...

Social behaviour and collective motion in plant-animal worms

“…B 283: 20152946 aggregations as living shields against environmental extremes, is seen, for example, in emperor penguins who form rotating huddles as protection against extreme Antarctic winds [30,31]. The worms are likely to find greater individual safety in these hugely dense aggregations and may even be able to defend themselves collectively through the mass production of dimethylsulfoniopropionate [8,32,33].…”

Chemotaxis by natural populations of coral reef bacteria

“…There is now evidence that both the coral symbionts Symbiodinium spp. (Keller et al, 1989;Broadbent et al, 2002) and the coral animal (Raina et al, 2013) have the capacity to produce significant quantities of DMSP. Our results confirm that, similar to other marine microorganisms (Miller et al, 2004;Seymour et al, 2010;Sharp et al, 2012), coralreef-associated bacteria use chemotaxis to enhance their access to DMSP or to follow DMSP gradients as a cue to locate the host (Garren et al, 2014).…”

“…There is evidence that the production and release of key chemoattractants, such as DMSP, can vary markedly under different environmental conditions and coral health states (Raina et al, 2013;Garren et al, 2014). From a bacterium's perspective, chemotaxis serves a variety of potential ecological functions, including (i) providing cells with greater access to important growth substrates and nutrients in otherwise oligotrophic habitats Seymour et al, 2009), (ii) enhancing exposure to terminal electron acceptors/donors (Schweinitzer and Josenhans, 2010) or (iii) use of infochemicals that may provide pathogenic microorganisms with information about the location, health and potential susceptibility of coral hosts to infection (Garren et al, 2014).…”

Rapid adaptive responses to climate change in corals

“…Another mechanism by which viruses could influence coral-associated bacterial communities is through genetic rearrangement. For example, shuffling of bacterial genes may result in wider metabolic potential, with coincident beneficial consequences for the coral host, for example, a broader range of products produced by dimethylsulfoniopropionate (DMSP)-metabolizing bacteria might enhance bacteria-mediated production of sulfur-based antimicrobials 97 . Despite such possible beneficial roles, however, viruses more typically have negative effects on host fitness and, in the case of corals, have been implicated in bleaching 98,99 and disease 100 .…”