Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum

Abstract

Mesodinium rubrum (Lohmann 1908) Jankowski 1976 (= Myrionecta rubra) is a common photosynthetic marine planktonic ciliate which can form coastal red-tides. It may represent a 'species complex' and since Darwin's voyage on the Beagle, it has been of great cytological, physiological and evolutionary interest. It is considered to be functionally a phytoplankter because it was thought to have lost the capacity to feed and possesses a highly modified algal endosymbiont. Whether M. rubrum is the result of a permanent endosymbiosis or a transient association between a ciliate and an alga is controversial. We conducted 'feeding' experiments to determine how exposure to a cryptophyte alga affects M. rubrum. Here we show that although M. rubrum lacks a cytostome (oral cavity), it ingests cryptophytes and steals their organelles, and may not maintain a permanent endosymbiont. M. rubrum does not fall into recognized cellular or functional categories, but may be a chimaera partially supported by organelle robbery.

Endosymbiotic associations within protists

“…Myrionecta rubra depends on ingestion of cryptophyte prey to sustain growth and a culture of the fragile ciliate was only successfully established when it was provided with the cryptophyte Teleaulax sp. (later determined to be G. cryophila; Johnson et al 2006) as prey (Gustafson et al 2000).…”

Ace Lake: three decades of research on a meromictic, Antarctic lake

“…It lacks a cell mouth or cytostome and derives all of its nutrition from a cryptophycean endosymbiont (Lindholm 1985). However, some investigators have shown that at least some members of the Mesodinium complex sequester plastids from cryptophycean prey (Gustafson et al 2000). In the mixolimnion of Ace Lake, M. rubrum can reach concentrations of up to 6 9 10 4 L -1 , but in other years numbers are lower, e.g.…”

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

“…While all strains of the ciliate that have been cultured require cryptophyte prey for sustained growth and maintenance of chlorophyll concentrations, disagreement exists as to the functional role of cryptophyte ingestion (Hansen and Fenchel 2006;Johnson et al 2007). Studies of a temperate strain of the ciliate (Hansen and Fenchel 2006) concluded that the association is symbiotic and stable, while research on an Antarctic strain (Gustafson et al 2000;Johnson et al 2007) described the association as unstable and a case of organelle retention. Perhaps the most tantalizing resolution to these competing views is that this species complex is in the process of undergoing a tertiary plastid acquisition, with certain strains retaining the ancestral trait of active organelle sequestration, due to an inability to divide the cryptophyte nucleus.…”

“…In this strain cryptophyte plastids possess identical nucleomorph and plastid SSU rRNA genes and pigment profiles to the free-living cultured prey of the ciliate, and thus appear to be sequestered by the ciliate (Johnson et al 2006). However, plastids in M. rubra undergo de novo division and pigment synthesis as long as the ciliate can continue to feed on cryptophyte prey (Gustafson et al 2000;Johnson and Stoecker 2005;Johnson et al 2007). The sequestered prey nucleus remains transcriptionally active within the ciliate for weeks, and has a half-life in the growing population of 10 days (Johnson et al 2007).…”