Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra

Abstract

It is well documented that organelles can be retained and used by predatory organisms, but in most cases such sequestrations are limited to plastids of algal prey. Furthermore, sequestrations of prey organelles are typically highly ephemeral as a result of the inability of the organelle to remain functional in the absence of numerous nuclear-encoded genes involved in its regulation, division and function. The marine photosynthetic ciliate Myrionecta rubra (Lohmann 1908) Jankowski 1976 (the same as Mesodinium rubrum) is known to possess organelles of cryptophyte origin, which has led to debate concerning their status as permanent symbiotic or temporary sequestered fixtures. Recently, M. rubra has been shown to steal plastids (that is, chloroplasts) from the cryptomonad, Geminigera cryophila, and prey nuclei were observed to accumulate after feeding. Here we show that cryptophyte nuclei in M. rubra are retained for up to 30 days, are transcriptionally active and service plastids derived from multiple cryptophyte cells. Expression of a cryptophyte nuclear-encoded gene involved in plastid function declined in M. rubra as the sequestered nuclei disappeared from the population. Cytokinesis, plastid performance and their replication are dependent on recurrent stealing of cryptophyte nuclei. Karyoklepty (from Greek karydi, kernel; kleftis, thief) represents a previously unknown evolutionary strategy for acquiring biochemical potential.

Endosymbiotic associations within protists

“…Interestingly, cryptophyte nuclei are also observed in M. rubra, but are sequestered independently from the plastidal complexes ( Johnson et al 2007). The cryptophyte nucleus retains its function for up to 30 days, is transcriptionally active and serves plastids derived from multiple cryptophyte cells ( Johnson et al 2007). Thus, the sequestered cryptophyte nuclei appear to regulate the cryptophyte organelle performance.…”

“…Loss of prey nuclei results in the inability of the plastids to divide, leading to a decline in organelle number and biochemical potential. Thus, M. rubra cells apparently depend on recurrent stealing of cryptophyte nuclei, a highly unusual lifestyle, termed 'karyoklepty' by Johnson et al (2007).…”

“…Thus, the sequestered cryptophyte nuclei appear to regulate the cryptophyte organelle performance. Because the retention time of prey nuclei is shorter than that for plastids, an average M. rubra cell may have eight cryptophyte plastids per single prey nucleus and prey nuclei need to be replaced by continuous feeding on cryptophyte algae ( Johnson et al 2007). Loss of prey nuclei results in the inability of the plastids to divide, leading to a decline in organelle number and biochemical potential.…”

Plastid Origin and Evolution

“…Similar heterotroph-autotroph kleptoplasty has also been observed between the heterotrophic and autotrophic dinoflagellates (Gast et al, 2007), the ciliates and the cryptomonad algae (Johnson et al, 2007), as well as between a number of foraminifera species and the diatoms (Bernhard and Bowser, 1999). Whereas the host sequestered only the plastids from preys in many cases, there are instances where the whole algal cell was maintained within the host (see Rumpho et al, 2011 for review).…”

Oxygenic photosynthesis and the distribution of chloroplasts

“…However, gene transfers between two very different Chl a/b algae to sea slug hosts have been demonstrated (Rumpho et al 2008;Pierce et al 2007). Another example from Stoecker's laboratory (Johnson et al 2007) highlights a ciliate that ''fed'' on flagellated cryptophytes and retained transcriptionally active cryptophyte nuclei. Such examples clearly suggest that transfer of genetic content is not uncommon among algal groups and hosts.…”