Marine planktonic ciliates that prey on macroalgae and enslave their chloroplasts

Abstract

Abstract-We found two tide-pool ciliates, Strombidium oculatum and Strombidium stylifer, that ingest ulvaceous green macroalgae and retain their chloroplasts. Sequences of the form I ribulose bisphosphate carboxylase/oxygenase (rubisco) large subunit gene (rbcL1) from chloroplasts found in the ciliates cluster with the Ulvophyceae sequences on GenBank and with those of ulvaceous macroalgae from pools in which the ciliates were collected. In addition, we have cultivated S. stylifer in vitro on filtered seawater supplemented with pieces of Enteromorpha thalli that had been treated with light and temperature shock to maximize production of reproductive unicells (swarmers). An average growth rate of 1.08 Ϯ 0.07 SE [standard error] d Ϫ1 was measured when S. stylifer was grown this way. Because both ciliates and the algal swarmers contain eyespots while vegetative cells in the Ulvophyceae do not, we speculate that these reproductive cells are the source of both the chloroplasts and the pigments used in the ciliates' eyespots. This ciliate will not grow in the dark and is required to ingest fresh chloroplasts every few days, making it an obligate mixotroph. Ingestion of macroalgae by ciliates constitutes an upside-down trophic link, contrary to the usual pattern for planktonic food webs, in which production passes from very small organisms to successively larger ones. Our finding suggests that macroalgal production, heretofore believed to contribute predominantly to detrital or macroherbivore food chains, may be an important food source in the nearshore plankton and that ciliates may play an important role in this trophic pathway.

Reframing the ‘Everything is everywhere’ debate: evidence for high gene flow and diversity in ciliate morphospecies

“…In S. stylifer, the adoral zone extends further down the ventral side than that of S. oculatum, and the girdle kinety of S. oculatum is closer to the mouth. Both species inhabit similar environments, contain a prominent eyespot, and are mixotrophs, harboring 'slave' chloroplasts derived from green macroalgae (McManus et al 2004).…”

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

“…Plastids in many oligotrich ciliates have a high turnover rate compared to other organelle-retaining protists, lasting only 9-40 h (Stoecker and Silver 1990), while those of L. strobila may persist for up to 14 days (Stoecker et al 1988) ( Table 2). The mixotrophic oligotrichs S. oculatum and S. stylifer have unusual trophic dynamics, stealing their plastids from the gametes of tide pool macroalgae (McManus et al 2004) (Fig. 1c).…”

“…(Ulvophyeae) reproductive tissue and/or gametes, but also the eye spot, creating a dense eyespot region in their own cell ( Fig. 1c; see reddish spot at cells base), likely used for phototaxis (McManus et al 2004). …”

Genetic Analyses of the rbcL and psaA Genes From Single Cells Demonstrate a Rhodophyte Origin of the Prey in the Toxic Benthic Dinoflagellate Ostreopsis

“…To further identify the prey, the ingested food particles were extracted from single Ostreopsis cells and their rbcL and psaA genes sequences were determined. These chloroplast-encoded genes have often been used to identify food particles inside protists such as dinoflagellates and ciliates (e.g., Hackett et al, 2003;McManus et al, 2004;Nishitani et al, 2010;Kim et al, 2012;Fawcett and Parrow, 2014). For example, McManus et al (2004) found through rbcL gene sequencing from chloroplasts found in the marine ciliates Strombidium oculatum and S. stylifer that the ciliates ingest ulvaceous green macroalgal swarmers and retain their chloroplasts.…”

“…These chloroplast-encoded genes have often been used to identify food particles inside protists such as dinoflagellates and ciliates (e.g., Hackett et al, 2003;McManus et al, 2004;Nishitani et al, 2010;Kim et al, 2012;Fawcett and Parrow, 2014). For example, McManus et al (2004) found through rbcL gene sequencing from chloroplasts found in the marine ciliates Strombidium oculatum and S. stylifer that the ciliates ingest ulvaceous green macroalgal swarmers and retain their chloroplasts. The psbA gene has also been applied to infer the origin and diversity of chloroplasts found in the mixotrophic dinoflagellate Dinophysis (e.g., Hackett et al, 2003;Nishitani et al, 2010;Kim et al, 2012).…”