Abstract
The prochlorophytes, oxygenic photosynthetic prokaryotes having no phycobiliprotein but possessing chlorophylls a and b, have been proposed to have a common ancestry with green chloroplasts, yet this is still controversal. We report here that partial sequence comparisons of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase, including sequence data from two prochlorophytes, Prochlorococcus and Prochloron, indicate that Prochlorococcus is more closely related to a photosynthetic bacterium, Chromatium vinosum (γ-purple bacteria), than to cyanobacteria, while Prochloron is closely related to the prochlorophyte Prochlorothrix and to cyanobacteria. The molecular phylogenetic tree indicates that a common ancestor of Prochlorococcus and γ-purple bacteria branched off from the land plant lineage earlier than Prochloron, Prochlorothrix, and cyanobacteria.
Similar content being viewed by others
References
Adachi J, Hasegawa M (1993) MOLPHY (programs for molecular phylogenetics) 2.1.1. Institute of Statistical Mathematics, Tokyo
Bej AK, Mahbubani MH, Dicesare JL, Atlas RM (1991) Polymerase chain reaction-gene probe detection of microorganisms by using filter-concentrated samples. Appl Environ Microbiol 57:3529–3534
Bold HC, Wynne MJ (1985) (eds) Introduction to the algae, 2nd ed. Prentice-Hall, New Jersey
Burger-Wiersma T, Matthijs HCP (1990) The biology of the Prochlorales. In: Codd GA, Dijkhuizen L, Tabita FR (eds) Autotrophic microbiology and one-carbon metabolism. Kluwer Academic Publishers, The Netherlands, pp 1–24
Burger-Wiersma T, Stal LJ, Mur LR (1989) Prochlorothrix hollandica gen. nov.: a filamentous oxygenic photoautotrophic prokaryote containing chlorophylls a and b: assignment to Prochlorothrichaceae fam. nov. and order Prochlorales Flonrenzano, Balloni and Materassi 1986, with emendation of the ordinal description. Int J Syst Bacteriol 39:250–257
Burger-Wiersma T, Veenhuis M, Korthals HJ, Van de Wiel CCM, Mur LR (1986) A new prokaryote containing chlorophylls a and b. Nature 320:262–264
Chisholm SW, Olson RJ, Zettler ER, Goericke R, Waterbury JB, Welschmeyer NA (1988) A novel free-living prochlorophyte abundant in the oceanic euphoric zone. Nature 334:340–343
Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, West-Johnsrud L, Zettler ER (1992) Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Archiv Microbiol 157:297–300
Curtis SE, Haselkorn R (1983) Isolation and sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 80: 1835–1839
Dionisio-Sese M, Shimada A, Maruyama T, Miyachi S (1993) Carbonic anhydrase activity of Prochloron sp. isolated from an ascidian host. Arch Microbiol 159:1–5
Dron M, Rahire M, Rochaix J-D (1982) Sequence of the chloroplast DNA region of Chlamydomonas reinhardii containing the gene of the large subunit of ribulose-1,5-bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162:775–793
Dzelzkalns VA, Szekeres M, Mulligan BJ (1988) The molecular biology of cyanobacteria. In: Shaw CH (ed) Plant molecular biology IRL, Washington, DC, pp 277–299
Felsenstein J (1993) PHYLIP (phylogeny inference package) 3.5.1c. University of Washington, Seattle, WA
Fujiwara S, Iwahashi H, Someya J, Nishikawa S (1993) Structure and cotranscription of the plastid-encoded rbcL and rbcS genes of Pleurochrysis carterae (Prymnesiophyta). J Phycol 29:347–355
Goericke R, Repeta DJ (1992) The pigments of Prochlorococcus marinus: the presence of divinyl chlorophyll a and b in a marine procaryote. Limnol Oceanogr 37:425–433
Golden SS, Morden CW, Greer KL (1993) Comparison of sequences and organization of photosynthesis genes among the prochlorophyte Prochlorothrix hollandica, cyanobacteria, and chloroplasts. In: Lewin RA (ed) Origins of plastids. Chapman & Hall, New York, pp 141–158
Hasegawa M, Hashimoto T (1993) Ribosomal RNA trees misleading? Nature 361:23
Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci 8:189–191
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160
Kusano T, Takeshima T, Inoue C, Sugawara K (1991) Evidence for two sets of structural genes coding for ribulose bisphosphate carboxylase in Thiobacillus ferrooxidans. J Bacteriol 173:7313–7323
Larkum AWD (1992) Evolution of chlorophylls, light harvesting systems and photoreaction centres. In: Murata N (ed) Research in photosynthesis, vol III. Kluwer Academic Publishers, The Netherlands, pp 475–482
Lewin RA (1975) A marine Synechocystis (Cyanophyta, Chroococcales) epizoic on ascidians. Phycologia 14:153–160
Lewin RA (1976) Prochlorophyta as a proposed new division of algae. Nature 261:697–698
Lewin RA (1977) Prochloron, type genus of the Prochlorophyta. Phycologia 16:217
Lewin RA (1981) Prochloron and the theory of symbiogenesis. Ann NY Acad Sci 361:325–329
Lewin RA, Cheng L (eds) (1989) Prochloron, a microbial enigma. Chapman & Hall, New York
Lewin RA, Withers NW (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256:735–737
Lockhart PJ, Beanland TJ, Howe CJ, Larkum AWD (1992) Sequence of Prochloron didemni atpBE and the inference of chloroplast origins. Proc Natl Acad Sci USA 89:2742–2746
Lockhart PJ, Penny D (1992) The problem of GC content, evolutionary trees and the origins of chl-a/b photosynthetic organelles: are the prochlorophytes a eubacterial model for higher plant photosynthesis? In: Murata N (ed) Research in photosynthesis, vol III. Kluwer Academic Publishers, The Netherlands, pp 499–505
MacKay RM, Salgado D, Bonen L, Stackebrandt E, Doolittle WF (1982) The 5S ribosomal RNAs of Paracoccus denitrificans and Prochloron. Nucleic Acids Res 10:2963–2970
Morden CW, Golden SS (1989a) psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337:382–385
Morden CW, Golden SS (1989b) psbA genes indicate common ancestry of prochlorophytes and chloroplasts, corrigendum. Nature 339:400
Morden CW, Golden SS (1991) Sequence analysis and phylogenetic reconstruction of the genes encoding the large and small subunits of ribulose-1,5-bisphosphate carboxylase/oxygenase from the chlorophyll b-containing prokaryote Prochlorothrix hollandica. J Mol Evol 32:379–395
Murata N, Sato N (1983) Analysis of lipids in Prochloron sp.: occurrence of monoglucosyl diacylglycerol. Plant Cell Physiol 24:133–138
Palenik B, Haselkorn R (1992) Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355:265–267
Ritland K, Clegg MT (1987) Evolutionary analysis of plant DNA sequences. Am Nat 130:S74–5100
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Seckbach J (1991) Systematic problems with Cyanidium caldarium and Galdieria sulphuraria and their implications for molecular biology studies. J Phycol 27:794–796
Seewaldt E, Stackebrandt E (1982) Partial sequence of 16S ribosomal RNA and the phylogeny of Prochloron. Nature 295:618–620
Shinozaki K, Yamada C, Takahata N, Sugiura M (1983) Molecular cloning and sequence analysis of the cyanobacterial gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 80:4050–4054
Swift H, Palenik B (1993) Prochlorophyte evolution and the origin of chloroplasts: morphological and molecular evidence. In: Lewin RA (ed) Origin of plastids. Chapman & Hall, New York, pp 123–139
Turner S, Burger-Wiersma T, Giovannoni SJ, Mur LR, Pace NR (1989) The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337:380–382
Ueda K, Shibuya H (1993) Molecular phylogeny of rbcL and its bearing on the origin of plastids: bacteria or cyanophyta? In: Sato S, Ishida M, Ishikawa H (eds) Endocytobiology V. Tübingen Univ. Press, Tübingen, pp 369–376
Urbach E, Robertson D, Chisholm SW (1992) Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355:267–270
Valentin K, Zetsche K (1990a) Nucleotide sequence of the gene for the large subunit of Rubisco from Cyanophora paradoxa—phylogenetic implications. Curr Genet 18:199–202
Valentin K, Zetsche K (1990b) Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222:425–430
Viale AM, Kobayashi H, Akazawa T (1989) Expressed genes for plant-type ribulose 1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium Chromatium vinosum, which possesses two complete sets of the genes. J Bacteriol 171:2391–2400
Yaguchi T, Chung SY, Igarashi Y, Kodama T (1993) Cloning, sequence and overexpression of the thermophilic cyanobacterium gene for the ribulose-1,5-bisphosphate carboxylase/oxygenase. J Ferment Bioeng 75:1–8
Withers NW, Vidaver W, Lewin RA (1978) Pigment composition, photosynthesis and fine structure of a non-blue-green prokaryotic algal symbiont (Prochloron sp.) in a didemnid ascidian from Hawaiian waters. Phycologia 17:167–171
Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271
Author information
Authors and Affiliations
Additional information
Correspondence to: A. Shimada
Rights and permissions
About this article
Cite this article
Shimada, A., Kanai, S. & Maruyama, T. Partial sequence of ribulose-1,5-bisphosphate carboxylase/oxygenase and the phylogeny of Prochloron and Prochlorococcus (Prochlorales). J Mol Evol 40, 671–677 (1995). https://doi.org/10.1007/BF00160516
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00160516