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Eubacteria, Halobacteria, and the Origin of Photosynthesis: the Photocytes (Evolution/Ribosome Structure/Parsimony/Eocytes/Eukaryotes) JAMES A

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Eubacteria, Halobacteria, and the Origin of Photosynthesis: the Photocytes (Evolution/Ribosome Structure/Parsimony/Eocytes/Eukaryotes) JAMES A 7154 Correction Proc. Natl. Acad. Sci. USA 82 (1985) Correction. In the article "Eubacteria, halobacteria, and the Natl. Acad. Sci. USA (82, 3716-3720), Fig. 1 was reproduced origin of photosynthesis: The photocytes" by James A. badly and an incorrect version of Fig. 6 was published. A Lake, Michael W. Clark, Eric Henderson, Shawn P. Fay, better reproduction of Fig. 1 and the correct version of Fig. Melanie Oakes, Andrew Scheinman, J. P. Thornber, and 6 are shown below. R. A. Mah, which appeared in number 11, June 1985, ofProc. Archae- Eo- Photocytes bacteria cytes (Photosynthesis) FIG. 6. Rooted evolutionary tree illustrating eubacteria and halobacteria as sublines of the monophyletic group, the photocytes. This tree shows the phylogenetic relationships among the photo- cytes, archaebacteria, and eocytes. The eubacterial and halobacte- rial branches of the photocytes are marked by diagonal lines. The possible photosynthetic common ancestor is indicated. This tree was ... ..'k rooted as described in ref. 5. 4i., . "*r'. ;$ V V.*- 11 FIG. 1. Electron micrographs of eubacterial (rows A-E) and halobacterial (rows F and G) ribosomal subunits. Small subunits in the asymmetric projection are shown in the first two columns, and large subunits in the quasi-symmetric projection (the L7/L12 stalk is to the right ofthe subunit) are shown in the third and fourth columns. The archaebacterial bills are indicated by arrows in rows F and G. The organisms represented are Chloroflexus aurantiacus (a green nonsulfur bacterium, row A), Thiocapsa pfennigii (a purple sulfur bacterium, row B), Rhodopseudomonas viridis (a purple nonsulfur bacterium, row C), Synechocystis 6701 (a cyanobacterium, row D), and Bacillus stearothermophilus (a nonphotosynthetic Gram-pos- itive thermophilic bacterium, row E). The halobacteria are Halobacterium cutirubrum (a halobacterium, row F) and Halococ- cus morrhuae (a halococcus, row G). (x225,000.) Downloaded by guest on October 2, 2021 Proc. Natl. Acad. Sci. USA Vol. 82, pp. 3716-3720, June 1985 Evolution Eubacteria, halobacteria, and the origin of photosynthesis: The photocytes (evolution/ribosome structure/parsimony/eocytes/eukaryotes) JAMES A. LAKE*, MICHAEL W. CLARK*, ERIC HENDERSON*, SHAWN P. FAY*, MELANIE OAKES*, ANDREW SCHEINMAN*, J. P. THORNBER*, AND R. A. MAHt *Molecular Biology Institute and Department of Biology, and tSchool of Public Health, University of California, Los Angeles, CA 90024 Communicated by Everett C. Olson, February 19, 1985 ABSTRACT The halobacteria and the photosynthetic ofphotosynthesis. This interpretation is supported by data on members of the eubacteria have previously been classified in the common denominators of photosynthesis, such as the two separate urkingdoms-the archaebacteria and the occurrence of identical types of carotenoids in both groups eubacteria, respectively. They were thought to be no more and their syntheses by essentially identical mechanisms (for closely related to each other than they each were to the reviews, see refs. 6 and 7). If this interpretation is correct, eukaryotes. In accord with this earlier classification, photo- then all halobacteria and all eubacteria, including synthesis was thought to have originated twice by independent nonphotosynthetic eubacteria, could be descendants of the events-once within the eubacteria and once within the same photosynthetic ancestor. archaebacteria. In this paper, however, using three- Evolutionarily, the eubacteria and halobacteria compose a dimensional ribosome structure as a probe of evolutionary monophyletic group, for which we propose the name divergences, we show that the eubacteria and the halobacteria "photocytes." As a group, the photocytes are more closely are more closely related to each other than they are to any other related to each other than they are to members of any other known organisms. The simplest interpretation of our data is urkingdom including the remaining archaebacteria that all extant photosynthetic cells are descended from a single (methanogens), the eukaryotes, or the eocytes. Hence, we common ancestor that possessed a primeval photosynthetic propose that halobacteria should be removed from the mechanism. Numerous data on the occurrence of related archaebacterial urkingdom and that urkingdom status be biochemical processes in halobacteria and eubacteria support given to the combined photosynthetic group, the "photo- this theory. Essential components of the photosynthetic ap- cyta," provided that other studies on their molecular proper- paratus, such as carotenoids, are present in both halobacteria ties confirm the proposed evolutionary tree. and in eubacteria, including the nonphotosynthetic eubacteria, suggesting that photosynthesis could be a primitive property of MATERIALS AND METHODS both groups. Our data indicate that together the eubacteria and the halobacteria form a monophyletic group for which we Ribosomes and ribosomal subunits from eubacteria, propose the name "photocytes." If other techniques of archaebacteria, eocytes, and eukaryotes were prepared as phylogenetic analysis cbnfirm this evolutionary tree, we pro- described (3, 5). Substitution of the buffer used to isolate pose that the photocytes be given urkingdom status. halobacterial ribosomes for that used to isolate eubacterial ribosomes produced no differences in ribosomal profiles. Photosynthetic bacteria have previously been classified in Subunits in these buffers were negatively stained by the two urkingdoms. The halobacteria are classified as double-layer carbon method. Relative sizes of eukaryotic, archaebacteria (1), whereas all other groups ofphotosynthet- archaebacterial, eocytic, and eubacterial subunits were de- ic bacteria are classified as eubacteria (2). As a result, it has termined by electron microscopy of pair-wise mixtures of been thought that photosynthesis was invented twice, once subunits from the groups. by archaebacteria and once by eubacteria. In this paper, we present evidence that photosynthesis, as exemplified by extant RESULTS photosynthetic bacteria, could have been invented once. Recently, techniques have been developed to use three- Electron micrographs of ribosomal subunits from repre- dimensional ribosome structure to probe evolutionary diver- sentative photosynthetic and nonphotosynthetic eubacteria gences and most parsimoniously to determine uprooted evolu- and from halobacteria are shown in Fig. 1. Small subunits are tionary trees (3-5). In particular, it has been shown that a rift, shown in the first two columns and large subunits are shown even deeper than that between the eubacteria and the in the last two columns. These are interpreted in diagrams separates the eocytes (a group of sulfur me- below the columns from each group. The small subunits are archaebacteria, shown in the "asymmetric projection" (8) and large subunits tabolizing bacteria) from the other bacteria (5). This prompted are shown in the "quasi-symmetric projection" (8). Both us to investigate the details of the relationship between the projections are particularly useful for comparative purposes methanogenic and halophilic branches of the archaebacteria and have been used previously to compare the three- and to analyze their specific relationships with eubacteria. dimensional structures of archaebacterial, eubacterial, In this paper, we present data showing that the eubacteria eocytic, and eukaryotic subunits (5, 9). and the halobacteria are more closely related to each other The representative photosynthetic eubacteria include a than they are to any other known organisms. We interpret green nonsulfur bacterium (row A), a purple sulfur bacterium this to imply that both could be derived from a common (row B), a purple nonsulfur bacterium (row C), and a photosynthetic ancestor corresponding to a single invention cyanobacterium (row D). For comparison, micrographs of a nonphotosynthetic Gram-positive bacterium are also in- The publication costs of this article were defrayed in part by page charge cluded (row E). Ribosomes from Halobacterium cutirubrum payment. This article must therefore be hereby marked "advertisement" and from Halococcus morrhuae are shown in rows F and G, in accordance with 18 U.S.C. §1734 solely to indicate this fact. respectively. The structures of the halobacterial ribosomal 3716 Evolution: Lake et al. Proc. Natl. Acad. Sci. USA 82 (1985) 3717 In contrast, ribosomes of methanogens, eocytes, and eukaryotes (Fig. 2) are distinctly different from the I eubacterial-halobacterial type (see Table 1). Their separate types (9) are illustrated beneath the micrographs in Fig. 2. Features present in the three types of small subunits but lacking, or present in a significantly modified form, in eubacterial and halobacterial subunits include lobes at the base of the subunit (nearly absent in methanogens, of intermediate size in eocytes, and large in eukaryotes), a bifurcation bf the platform, and d gap at the base of the platform. Fields of small subunits from a methanogen, a eubacterium, and a halobacterium are shown from left to right, respectively, in Fig. 3. In large ribosomal subunits two features, lacking in eubacteria and halobacteria, are present in subunits from eocytes and eukaryotes. These are a lobe at the base ofthe subunits and a prominent bulge above the lobe and separated from it by a gap in eocytes. The gap is filled in eukaryotes. The profiles of the eocytic subunits, where they I l cQ I I I FIG. 1. Electron micrographs of eubacterial (rows A-E) and halobacterial (rows F and G) ribosomal
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