From endosymbiosis to synthetic photosynthetic life.

The chloroplasts of photosynthetic eukaryotes arose more than 1.6 billion years ago (Yoon et al., 2004) through the process of primary endosymbiosis, in which a cyanobacterium became permanently integrated into a heterotrophic mitochondriate eukaryote (Reyes-Prieto et al., 2007). Through subsequent secondary and tertiary endosymbioses (i.e. additional nested endosymbioses between plastid-bearing eukaryotes), plastids spread out into a vast array of photosynthetic and nonphotosynthetic organisms, the former contributing a large share of the global primary productivity and the latter encompassing a huge diversity of organisms ranging from the protists that cause malaria to parasitic plants. Thus, the plastids in nearly all present-day plastid-bearing organisms descended from a single primary endosymbiosis (Gould et al., 2008; Archibald, 2009; Keeling, 2010). Considering that endosymbiotic relationships between bacteria and eukaryotes are common in nature (Nowack and Melkonian, 2010), it is remarkable that only one such primary association between cyanobacterium and host apparently took hold in ancient evolutionary history to produce a bona fide chloroplast and spawn the diversity of plastid-bearing organisms now extant on earth. Evidence for more recent endosymbioses leading toward the evolution of new primary plastids (Prechtl et al., 2004; Gould et al., 2008; Nowack et al., 2008; Archibald, 2009) indicate that the establishment of more such associations is possible, but the evolutionary transition from cyanobiont to organelle is extraordinarily rare. In contrast, secondary and tertiary endosymbioses yielding new types of plastid-bearing organisms have occurred multiple times (Gould et al., 2008; Keeling, 2010). This raises the intriguing question: What does it take to establish a permanent and functional plastid in a foreign host? As many aspects of plastid research are directly or indirectly rooted in the endosymbiotic origin of these organelles, continued pursuit of this question from various perspectives holds potential for illuminating a great deal about how plastid function is integrated with that of the host organism, which is still poorly understood. Here we highlight recent findings bearing on this question and consider novel approaches that could help provide answers. The requirements for evolving a plastid in a host cell have been discussed in many reviews (e.g. Bhattacharya et al., 2007; Gould et al., 2008). Photosynthesis probably catalyzed evolution of the first plastids by providing reduced carbon to the host cell, thereby reducing or eliminating the need for feeding (Weber et al., 2006; Nowack and Melkonian, 2010). A stunning example of the significance of photosynthesis in this context is the kleptoplastic association between the sea slug Elysia chlorotica and the heterokont alga Vaucheria litorea (Rumpho et al., 2006). E. chlorotica sucks chloroplasts out of the algal cells, harbors them in the cytosol of cells lining the digestive track (Kawaguti and Yamasu, 1965; Taylor, 1967), and completes its life cycle photoautotrophically, with no additional ingestion of organic food sources. In fact, though this cannot be considered a permanent association because the plastids cannot divide or be transmitted to the next generation, the captured chloroplasts are maintained in a photosynthetically active state for up to 14 months. Since many components of the photosynthetic machinery have high turnover rates and must be frequently replaced with newly synthesized proteins, several potential explanations for kleptoplast longevity in the slug were considered, including the possibility that the algal plastid genome contains all the required genes (Green et al., 2000; Rumpho et al., 2000). However, while it was found that kleptoplast genes are expressed for at least 8 months in starved slugs (Mujer et al., 1996), sequence analysis showed that at least one gene required for photosynthetic electron transport was missing from the algal plastid genome and that the corresponding protein must therefore be provided by the slug (Rumpho et al., 2008). Indeed, a number of genes required for photosynthesis reside in the sea slug nucleus and were acquired from the alga by horizontal gene transfer (Pierce et al., 2007; Rumpho et al., 2009; Schwartz et al., 2010). Presumably the encoded proteins are targeted to the kleptoplast via the plastid import machinery, though this remains to be shown experimentally. With recent progress in genome sequencing technology, in the near future comparison of the E. chlorotica and V. litorea nuclear genomes should make it relatively straightforward to identify the full complement of algal genes transferred to the slug that may be critical 1 This work was supported by the German Research Council (grant nos. DFG WE 2231/4–1, SFB TR1, and IRTG 1525/1 to A.P.M.W.), by the National Science Foundation (grant nos. 0544676 and 0519740 to K.W.O.), and by the U.S. Department of Energy (grant no. DE–FG02–06ER15808 to K.W.O.). 2 These authors contributed equally to the article. * Corresponding author; e-mail [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.110.161216