Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium

Abstract

Survival of free-living and symbiotic dinoflagellates (Symbiodinium spp.) in coral reefs is critical to the maintenance of a healthy coral community. Most coral reefs exist in oligotrophic waters, and their survival strategy in such nutrient-depleted waters remains largely unknown. In this study, we found that two strains of Symbiodinium spp. cultured from the environment and acquired from the tissues of the coral Alveopora japonica had the ability to feed heterotrophically. Symbiodinium spp. fed on heterotrophic bacteria, cyanobacteria (Synechococcus spp.), and small microalgae in both nutrient-replete and nutrient-depleted conditions. Cultured free-living Symbiodinium spp. displayed no autotrophic growth under nitrogen-depleted conditions, but grew when provided with prey. Our results indicate that Symbiodinium spp.'s mixotrophic activity greatly increases their chance of survival and their population growth under nitrogen-depleted conditions, which tend to prevail in coral habitats. In particular, free-living Symbiodinium cells acquired considerable nitrogen from algal prey, comparable to or greater than the direct uptake of ammonium, nitrate, nitrite, or urea. In addition, freeliving Symbiodinium spp. can be a sink for planktonic cyanobacteria (Synechococcus spp.) and remove substantial portions of Synechococcus populations from coral reef waters. Our discovery of Symbiodinium's feeding alters our conventional views of the survival strategies of photosynthetic Symbiodinium and corals. mixotrophy | zooxanthella | coral bleaching | food web | Heterosigma

Symbiodinium necroappetenssp. nov. (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals

“…Various cultured Symbiodinium exhibit chemo-tropism to nitrogenous sources (Fitt, 1984), and therefore many Symbiodinium may exhibit greater mixotrophy without direct access to host inorganic nitrogen. Furthermore, Symbiodinium are capable of feeding phagotrophically on bacteria (Jeong et al, 2012). We propose that under natural conditions S. necroappetens may depend on mixotrophy more than 'symbiotic' species and that damaged or diseased tissues provide fleeting sources of food either through the uptake of inorganic compounds (D'Elia et al, 1983) or by consuming bacteria associated with tissue decomposition.…”

Unfolding the secrets of coral–algal symbiosis

“…Dinoflagellates are important microbial eukaryotes that, together with diatoms, are the leading primary producers in the oceans (Lin, 2011), although recent studies suggest that dinoflagellates of the genus Symbiodinium are also capable of heterotrophy (Jeong et al, 2012). Dinoflagellates are characterized by a very large genome (Hackett et al, 2004) and a number of unique features such as DNA containing 5-hydoxymethylmuracil (Rae, 1976), a lack of the usual histones (Rizzo, 1981) and transcriptional regulatory elements (Li and Hastings, 1998).…”

Current Knowledge and Recent Advances in Marine Dinoflagellate Transcriptomic Research

“…Dinoflagellates are found in a range of marine ecosystems including estuaries, mangroves and deep-sea environments, and some exist as symbionts with other organism such as coral and epiphytes of seaweeds and seagrass [2][3][4][5][6]. Their lifestyle ranges from mixotrophic through to heterotrophic and autotrophic [7][8][9]. They also have been reported to be the major cause of the harmful algae blooms (HABs), sometimes referred to as 'red tide' events in the ocean, and may result in death of marine mammals and affect human health due to the accumulative effect of toxins moving throughout the food chain when contaminated seafood is consumed [10,11].…”