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Evidence That Cryptomonad Chloroplasts Evolved from Photosynthetic Eukaryotic Endosymbionts

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Evidence That Cryptomonad Chloroplasts Evolved from Photosynthetic Eukaryotic Endosymbionts Evidence that cryptomonad chloroplasts evolved from photosynthetic eukaryotic endosymbionts GEOFFREY IAN McFADDEN Plant Cell Biology Research Centre, School of Botany, University of Melbourne, Parkville, Victoria 3052, Australia Summary Unicellular algae of the division Cryptophyta pos- the rRNAs may be transcribed from genes in this sess an unusual subcellular compartment of un- nucleus. This identification of a second, nucleus- known derivation. This compartment, which is containing eukaryotic compartment within these partitioned off from the main cytoplasm by two cells supports the hypothesis that cryptomonads membranes, contains a chloroplast and a small contain a reduced photosynthetic eukaryotic endo- nucleus-like organelle surrounded by ribosome- symbiont. like particles. Electron-microscopic in situ hybrid- ization has been used to show that the ribosomes in this subcellular compartment are eukaryotic. In addition, eukaryotic rRNA has been localised Key words: chloroplasts, cryptomonads, endosymbiosis, /;; within the nucleus-like organelle, suggesting that situ hybridization, ribosomes, ribosomal RNA. Introduction main supporting evidence for this hypothesis is that chloroplasts in these algae are surrounded by four mem- Photosynthesis evolved in prokaryotes (Krishna Rao et branes (Gibbs, 19816). The inner pair of membranes is al. 1985) and was acquired by eukaryotes through endo- considered homologous to the green plant chloroplast symbiosis of a prokaryote (Margulis, 1981; Taylor, 1987; envelopes (Whatley, 1981; Whatley et al. 1979; Cavalier- Gray, 1988; Giovannonieia/. 1988). The photosynthetic Smith, 1986). The two outer membranes are termed the prokaryotic endosymbiont in green plants has been chloroplast endoplasmic reticulum (CER) (Gibbs, reduced to a semi-autonomous organelle bound by two 19816). The outermost CER membrane, which is usually membranes, the chloroplast. The inner chloroplast mem- continuous with the nuclear envelope/rough endoplas- brane probably represents the endosymbiont's plasma mic reticulum and bears eukaryotic ribosomes, is putati- membrane, while the outer membrane could be derived vely derived from the endomembrane system of the host from the outer membrane of the endosymbiont (Cavalier- cell, while the inner CER membrane could represent the Smith, 1987) or the phagocytotic vacuole of the host cell plasma membrane of the eukaryotic endosymbiont (Whatley and Whatley, 1981; Whatley et al. 1979; (Whatley and Whatley, 1981; Dodge, 1979; Cavalier- Dodge, 1979). It is envisaged that many of the endosym- Smith, 1986). biont's genes were transferred to the host cell nucleus One group from the Kingdom Chromista, the crypto- (Harrington and Thornley, 1982; Weeden, 1981), monads, may be an intermediate stage in the reduction of thereby stabilizing the symbiotic relationship and con- a photosynthetic eukaryotic endosymbiont to a chloro- verting the endosymbiont to a true organelle (Cavalier- plast with four limiting membranes. Cryptomonads Smith and Lee, 1985). (Division Cryptophyta) are common marine or fresh- Photosynthetic algae of the Kingdom Chromista water biflagellates (Gantt, 1980). Between the inner and (Cavalier-Smith, 1986) (e.g. diatoms, brown algae, gol- outer pairs of membranes surrounding the chloroplast in den flagellates, cryptomonads) are thought to have cryptomonad cells is a small compartment termed the acquired their chloroplasts 'third hand'. According to this periplastidal space, which contains ribosome-like par- hypothesis (illustrated in Fig. 1), a photosynthetic pro- ticles and a small organelle resembling a nucleus, known karyote became a chloroplast in an unknown eukaryotic as the nucleomorph (Greenwood, 1974; see Fig. 2, this intermediary, which in turn became an endosymbiont paper). It has been proposed that the nucleomorph is a within a second phagotroph (Greenwood et al. 1977; vestigial nucleus from a eukaryotic endosymbiont and Whatley and Whatley, 1981; Whatley et al. 1979; Dodge, that the ribosome-like particles in the periplastidal space 1979; Cavalier-Smith, 1982, 1986; Gibbs, 1981a). The are ribosomes from the endosymbiont's cytoplasm Journal of Cell Science 95, 303-308 (1990) Printed in Great Britain © The Company of Biologists Limited 1990 303 Fig. 1. Hypothetical sequence of endosymbioses in evolution of cryptomonads (see text for references). A photosynthetic prokaryote (Pr) was engulfed by an unknown eukaryote (Eul) and became a chloroplast in an unidentified photosynthetic eukaryote. The photosynthetic eukaryote was in turn engulfed by a second phagotroph (Eu2) and became an endosymbiont to create autotrophs like cryptomonads. Vestiges of the nucleus and cytoplasm of the photosynthetic eukaryotic endosymbiont (Eul) would be retained in a subcellular compartment of the second host. In situ hybridization studies reported here identify this compartment as containing eukaryotic ribosomes. Preliminary evidence suggests that rRNA for these ribosomes may be encoded by a second nucleus derived from the eukaryotic endosymbiont (Eul). (i.e. those in the chloroplast) or eukaryotic origin (nu- clear-encoded cytoplasmic ribosomes) by electron mi- croscopy (McFadden et al. 1988; McFadden, 1989). I have examined cryptomonads by high-resolution in situ hybridization using two probes, one specific for eukary- otic ribosomal RNA (rRNA) and the other specific for prokaryotic rRNA. The ribosomes in the periplastidal space are shown to be eukaryotic and are quite probably transcribed from genes in the nucleomorph. Materials and methods Cultures The cryptomonad (Chroomonas caudata Geitler, Melbourne University Culture Collection no. CrlO) was grown under a fluorescent illumination in WARIS-H media as described Periplastidal \~ // Chloro space (McFadden and Melkonian, 1986). The bacteria (Bacillus sp.) Cytoplasm were contaminants in one of the algal sub-cultures. Standard electron microscopy Cells were fixed in 2% glutaraldehyde in 50mM-piperazine- Ar,A''-bis[2]-ethanesulphonic acid (pH7) at 4°C for one hour. Cells were then post-fixed in 1 % OsCj and embedded in Spurr's resin. In situ hybridization fixation Fig. 2. Diagram showing subcellular compartments in a For in situ hybridization the cells were fixed in glutaraldehyde cryptomonad. At the anterior is a gullet with two emergent as above, washed in the buffer, dehydrated to 70% ethanol and flagella. The main nucleus with its nucleolus (No) is at the embedded in LR Gold resin (McFadden et al. 1988). Fixation posterior. Four membranes surround the chloroplast. An with OsO4 is not compatible with in situ hybridization (McFad- extension of the nuclear membranes, the chloroplast den, 1989). endoplasmic reticulum (CER), envelopes the chloroplast and associated compartment. Between the CER and the Probes chloroplast envelopes is the periplastidal space, which The eukaryotic rRNA probe was a 1000 bp (base pair) BamHl/ contains ribosome-like particles and the nucleomorph. Bar, EcoRl nuclear genomic fragment of the 18 S rRNA gene from 1 /tm. Pisum sativum (Jorgensen et al. 1987). The prokaryotic rRNA probe was an 800 bp EcoRl fragment partially encoding 16 S rRNA from the chloroplast genome of Chlamydomonas rein- (Greenwood et al. 1977; Whatley and Whatley, 1981; hardtii (Eco 36/37, according to Grant et al. 1980). Whatley <?* a/. 1979; Dodge, 1979; Cavalier-Smith, 1982, 1986; Gibbs, 1981a). In situ hybridization A test of the eukaryotic endosymbiont hypothesis is to Biotinylated sense and antisense RNA probes were prepared show that the ribosomes in the periplastidal compartment using bio-11-rUTP and in vitro transcription vectors as de- of crytptomonads are eukaryotic, and that the nucleo- scribed (McFadden, 1989). Probes were hybridized to ultrathin morph encodes components of these ribosomes. Recent sections (100 nm thick) at a very high stringency at 65 °C in a advances in in situ hybridization technology permit the buffer containing 50% formamide and 0.15M-NaCl (McFad- identification of ribosomes of either prokaryotic origin den et al. 1988) then washed in 0.15M-NaCl at 65°C for 2h. 304 G. I. McFadden Hybrids were detected with anti-biotin antibody and a second- Cryptomonads ary antibody conjugated to colloidal gold as previously de- The general morphology and physiology of cryptomo- scribed (McFadden, 1989). nads is described in detail elsewhere (Gantt, 1980). Briefly, cryptomonads are small, bean-shaped biflagel- Results lates containing chlorophylls a and Cz plus phycobilipro- teins. Fig. 2 illustrates the compartmentation in a crypto- Specificity of the probes monad cell. The chloroplast is bounded by four membranes (Fig. 2). Between the inner and outer pairs At the stringency used, the prokaryotic probe hybridizes of membranes is the periplastidal compartment (Figs 2 only with prokaryotic rRNA and the eukaryotic probe and 5), which contains ribosome-like particles and the hybridizes only with eukaryotic rRNA. Fig. 3 shows the nucleomorph (Figs 2 and 5). The nucleomorph is two probes hybridized to bacteria. The prokaryotic probe bounded by a double membrane with pores and has an labels ribosomes in the cytoplasm of bacterial cells electron-opaque zone resembling a nucleolus plus several (Fig. 3A) but the eukaryotic probe does not label bac- smaller electron-dense globules (Fig. 5D). terial ribosomes (Fig. 3B). Fig. 5 shows the periplastidal compartment of crypto- Fig. 4 shows the two probes hybridized to cryptomo- monad cell and labelling of the compartment with the nad cells. The prokaryotic probe labels only the ribo-
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