Mesodinium rubrum: The symbiosis that wasn’t

Qiu et al. (1) report that a red tide of the photosynthetic ciliate Mesodinium rubrum in Long Island Sound “farms” symbiotic Teleaulax amphioxeia cells within its cytoplasm. M. rubrum has long been studied for causing red tides (2⇓⇓–5), and laboratory culture work on multiple strains from around the world has shown that M. rubrum extracts organelles from ingested cryptophyte algae, including chloroplasts, mitochondria, cytoplasm, and a transcriptionally active nucleus, or kleptokaryon (6, 7). M. rubrum functions like a true phototroph, with the ability to regulate and divide chloroplasts (7).

The conclusions of Qiu et al. (1), based on a single field sample, contrast sharply with these previously published studies of M. rubrum. Their conclusions are based on (i) their inference that “complete” prey metatranscriptomes indicate metabolically intact prey cells and (ii) their visual observation, using transmission electron microscopy (TEM), of intact prey cells. However, we believe that these findings do not provide sufficient evidence to support the extraordinary claim by Qiu et al. (1) that M. rubrum farms prey cells.

First, the authors argue that the expression of genes involved in membrane transporters, nucleus-to-cytoplasm RNA transporters, and all major metabolic pathways is evidence of intact cryptophyte symbionts. Here we show data from a temperate strain of M. rubrum (clade G) that indicate that many cryptophyte gene pathways are expressed at levels equal to or greater than in T. amphioxeia even when only prey organelles remain (Table 1 and Fig. 1). One exception is expression levels of ABC-like transporters, which were observed to be at even lower numbers in Qui et al. (1). Furthermore, we have previously shown similar transcriptional patterns of highly expressed cryptophyte genes in an Antarctic M. rubrum culture (clade A) (8). In addition, because genomes or transcriptomes of the target organisms were not used for annotation (1) there is a high degree of uncertainty in assigning transcript identity.

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Fig. 1.

Transmission electron micrograph of Mesodinium rubrum (CBJR05; clade G) fed T. amphioxeia (GCEP01). The image shows a lateral cross-section of an M. rubrum cell revealing at least nine plastid complexes and a recently ingested T. amphioxeia cell (also a cross-section) within a vacuole (white arrow) in the center. Note the ingested cell’s periplast membrane and cytoplasm surrounding the chloroplast, and the vacuolar space surrounding it. In this image the cytoplasm of the cryptophyte organelle complexes is lighter than that of the ciliate, revealing that large portions of M. rubrum cells are devoted to hosting stolen organelles. Ciliate cytoplasm and many of the organelles in the image of Qiu et al. (1) are missing or unrecognizable, respectively.

Second, Qiu et al. (1) report intact cryptophyte cells inside M. rubrum. However, their TEM images are inconclusive due to (i) low resolution (ii), extraordinarily poor fixation quality, and (iii) unusually small cryptophyte organelles, compounding the interpretation of the low-resolution images. No clear cell membrane, which would include cytoplasm completely surrounding the chloroplast, is visible around the cryptophyte organelles in their images. Rather, they seem to be organelle complexes that are packed into a membrane, consistent with previous observations (9). Furthermore, in other M. rubrum recently ingested intact cryptophytes seem to be in a vacuole before organelle extraction (Fig. 1) (10).

M. rubrum-like ciliates are complex organisms that do not fit into established “boxes” for trophic modes or cellular organization. However, we have previously shown that their unique mode of acquired phototrophy is capable of “farming” cryptophyte organelles when the kleptokaryon is present (7), and there is no evidence for maintenance of intact symbionts within any cultures of the ciliate. We firmly believe that the conclusions of Qiu et al. (1) do not represent a new association in M. rubrum but rather illustrate the actual difficulties of accurately interpreting “snapshots” of natural populations.