The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics

Wolfgang R. Hess1,2, Gabrielle Rocap3, Claire S. Ting4, Frank Larimer5, Stephanie Stilwagen6, Jane Lamerdin6, Sallie W. Chisholm4,3
1Humboldt-University Berlin, Germany
2Institute of Biology, Berlin, Germany
3Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, USA
4Department of Biology, Massachusetts Institute of Technology, Cambridge, USA
5Computational Biology, Oak Ridge National Laboratory, Oak Ridge, USA
6DOE Joint Genome Institute, Walnut Creek, USA

Tóm tắt

Within the vast oceanic gyres, a significant fraction of the total chlorophyll belongs to the light-harvesting antenna systems of a single genus, Prochlorococcus. This organism, discovered only about 10 years ago, is an extremely small, Chl b-containing cyanobacterium that sometimes constitutes up to 50% of the photosynthetic biomass in the oceans. Various Prochlorococcus strains are known to have significantly different conditions for optimal growth and survival. Strains which dominate the surface waters, for example, have an irradiance optimum for photosynthesis of 200 μmol photons m−2 s−1, whereas those that dominate the deeper waters photosynthesize optimally at 30–50 μmol photons m−2 s−1. These high and low light adapted ‘ecotypes’ are very closely related — less than 3% divergent in their 16S rRNA sequences — inviting speculation as to what features of their photosynthetic mechanisms might account for the differences in photosynthetic performance. Here, we compare information obtained from the complete genome sequences of two Prochlorococcus strains, with special emphasis on genes for the photosynthetic apparatus. These two strains, Prochlorococcus MED4 and MIT 9313, are representatives of high- and low-light adapted ecotypes, characterized by their low or high Chl b/a ratio, respectively. Both genomes appear to be significantly smaller (1700 and 2400 kbp) than those of other cyanobacteria, and the low-light-adapted strain has significantly more genes than its high light counterpart. In keeping with their comparative light-dependent physiologies, MED4 has many more genes encoding putative high-light-inducible proteins (HLIP) and photolyases to repair UV-induced DNA damage, whereas MIT 9313 possesses more genes associated with the photosynthetic apparatus. These include two pcb genes encoding Chl-binding proteins and a second copy of the gene psbA, encoding the Photosystem II reaction center protein D1. In addition, MIT 9313 contains a gene cluster to produce chromophorylated phycoerythrin. The latter represents an intermediate form between the phycobiliproteins of non-Chl b containing cyanobacteria and an extremely modified β phycoerythrin as the sole derivative of phycobiliproteins still present in MED4. Intriguing features found in both Prochlorococcus strains include a gene cluster for Rubisco and carboxysomal proteins that is likely of non-cyanobacterial origin and two genes for a putative $$\varepsilon$$ and β lycopene cyclase, respectively, explaining how Prochlorococcus may synthesize the α branch of carotenoids that are common in green organisms but not in other cyanobacteria.

Từ khóa


Tài liệu tham khảo

Adamska I, Ohad I and Kloppstech K (1992) Synthesis of the early light-inducible protein is controlled by blue light and related to light stress. Proc Natl Acad Sci USA 89: 2610–2613

Apt KE, Collier JL and Grossman AR (1995) Evolution of the phycobiliproteins. J Mol Biol 248: 79–96

Armstrong GA (1994) Eubacteria show their true colors: Genetics of carotenoid pigment biosynthesis from microbes to plants. J Bacteriol 176: 4795–4802

Bouyoub A, Vernotte C and Astier C (1993) Functional analysis of the two homologous psbA gene copies in Synechocystis PCC 6714 and PCC 6803. Plant Mol Biol 21: 149–258

Burger-Wiersma T, Veenhuis M, Korthals HJ, Van de Wiel CCM and Mur LR (1986) A new prokaryote containing chlorophylls a and b. Nature 320: 262–264

Bustos SA and Golden SS (1992) Light-regulated expression of the psbD gene family in Synechococcus sp. strain PCC 7942: Evidence for the role of duplicatedpsbD genes in cyanobacteria. Mol Gen Genet 232: 221–230

Chisholm SW, Olson RJ, Zettler ER, Waterbury J, Goericke R and Welschmeyer N (1988) A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. Nature 334: 340–343

Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, West-Johnsrud L and Zettler ER (1992) Prochlorococcus marinus nov. gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch Microbiol 157: 297–300

Collier JL and Grossman AR (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13: 1039–1047

Colon-Lopez MS and Sherman LA (1998) Transcriptional and translational regulation of Photosystem I and II genes in lightdark-and continuous-light-grown cultures of the unicellular cyanobacterium Cyanothece sp. strain ATCC 51142. J Bacteriol 180: 519–526

Cornejo J, Willows RD and Beale SI (1998) Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxindependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J 15: 99–107

Cunningham FX and Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49: 557–583

Cunningham FX, Sun Z, Chamovitz D, Hirschberg J and Gantt E (1994) Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp. strain PCC7942. Plant Cell 6: 1107–1121

Cunningham FX, Pogson B, Sun Z, McDonald KA, DellaPenna D and Gantt E (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes ofArabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8: 1613–1626

Delwiche CF and Palmer JD (1996) Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol 13: 873–882.

Dolganov NA, Bhaya D and Grossman AR (1995) Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc Natl Acad Sci USA 92: 636–640

Frankenberg N, Mukougawa K, Kohchi T and Lagarias JC (2001) Functional genomic analysis of the HY2 family of ferredoxindependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13: 965–978

Garczarek L, Hess WR, Holtzendorff J, Van der Staay GWM and Partensky F (2000) Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc Natl Acad Sci USA 97: 4098–4101

Garczarek L, Partensky F, Holtzendorff J, Babin M, Mary I, Thomas JC and Hess WR (2001) Differential expression of antenna and core genes in the marine oxychlorobacterium Prochlorococccus PCC 9511 grown under light-dark cycles. Environ Microbiol 3: 168–175

Gingrich JC, Buzby JS, Stirewalt VL and Bryant DA (1988) Genetic analysis of two new mutations resulting in herbicide resistance in the cyanobacterium Synechococcus sp. PCC 7002. Photosynth Res 16: 83–99

Gingrich JC, Gasparich GE, Saver K and Bryant DA (1990) Nucleotide sequence and expression of the two genes encoding D2 protein and the single gene encoding the CP43 protein of Photosystem II in the cyanobacterium Synechococcus sp. PCC 7002. Photosynth Res 24: 137–150

Glass JI, Lefkowitz EJ, Glass JS, Heiner CR, Chen EY and Cassell GH (2000) The complete sequence of the mucosal pathogen Ureaplasma urealyticum. Nature 407: 757–762

Goericke R and Repeta DJ (1992) The pigments of Prochlorococcus marinus: the presence of divinyl chlorophyll a and b in a marine prochlorophyte. Limnol Oceanogr 37: 425–433

Goericke R and Welschmeyer NA (1993) The Marine Prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res 40: 2283–2294

Goericke R, Olson RJ and Shalapyonok A (2000) A novel niche for Prochlorococcus sp. in low-light suboxic environments in the Arabian Sea and the eastern tropical North Pacific. Deep Sea Res I 47: 1183–1205

Golden SS and Stearns GW (1988) Nucleotide sequence and transcript analysis of three Photosystem II genes from the cyanobacterium Synechococcus sp. PCC7942. Gene 67: 85–96

Golden SS, Brusslan J and Haselkorn R (1986) Expression of a family of psbA genes encoding a Photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5: 2789–2798

Gotz T, Windhovel U, Boger P and Sandmann G (1999) Protection of photosynthesis against ultraviolet-B radiation by carotenoids in transformants of the cyanobacterium Synechococcus PCC7942. Plant Physiol 120: 599–604

Green BR and Kuhlbrandt W(1995) Sequence conservation of lightharvesting and stress-response proteins in relation to the threedimensional molecular structure of LHC II. Photosynth Res 44: 139–148

Green BR and Pichersky E (1994) Hypothesis for the evolution of three-helix Chl a/b and Chl a/c light-harvesting antenna proteins from two-helix and four-helix ancestors. Photosynth Res 39: 149–162

Grimm B and Kloppstech K (1987) The early light-inducible proteins of barley. Characterization of two families of 2-h-specific nuclear-coded chloroplast proteins. Eur J Biochem 167: 493–499

He Q, Dolganov N, Bjorkman O and Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276: 306–314

Heddad M and Adamska I (2000) Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/bbinding gene family. Proc Natl Acad Sci USA 97: 3741–3746

Hess WR (1997) Localization of an open reading frame with homology to human aspartoacylase upstream from psbA in the prokaryote Prochlorococcus marinus CCMP 1375. DNA Seq 7: 301–306

Hess WR and Partensky F (1999) Analysis of a phycobiliprotein gene cluster in Prochlorococcus marinus CCMP 1375: Identification of a putative linker polypeptide and the phylogeny of Prochlorococcus phycoerythrins In: Peschek GA, Löffelhardt W and Schmetterer G (eds) The Photosynthetic Prokaryotes, pp 751–761. Plenum Press, New York

Hess WR, Weihe A, Loiseaux-de Goer S, Partensky F and Vaulot D (1995) Characterization of the single psbA gene of Prochlorococcus marinus CCMP 1375 (Prochlorophyta). Plant Mol Biol 27: 1189–1196

Hess WR, Partensky F, Van der Staay GW, Garcia- Fernandez JM, Börner T and Vaulot D (1996) Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc Natl Acad Sci USA 93: 11126–11130

Hess WR, Steglich C, Lichtlé C and Partensky F (1999) Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membranes and are encoded by a single large gene cluster. Plant Mol Biol 40: 507–521

Holthuijzen Y A, Van Breeman JFL, Konings WN and van Bruggen EFJ (1986a) Electron microscopic studies of carboxysomes in Thiobacillus neapolitanus. Arch Microbiol 144: 258–262

Holthuijzen YA, Van Breeman JFL, Kuenen JG and Konings WN (1986b) Protein composition of the of carboxysomes of Thiobacillus neapolitanus. Arch Microbiol 144: 398–404

Jansson S, Andersson J, Kim SJ and Jackowski G (2000) An Arabidopsis thaliana protein homologous to cyanobacterial highlight-inducible proteins. Plant Mol Biol 42: 345–351

Johnson Z, Landry ML, Bidigare RR, Brown SL, Campbell L, Gunderson J, Marra J and Trees C (1999) Energetics and growth kinetics of a deep Prochlorococcus spp. population in the Arabian Sea. Deep Sea Res II 46: 1719–1743

Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement). DNA Res 3: 185–209

Kaplan A and Reinhold L (1999)CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539–570

Kehoe DM and Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409–1412

Klughammer B, Sultemeyer D, Badger MR and Price GD (1999) The involvement of NAD(P)H dehydrogenase subunits, NdhD3 and NdhF3, in high-affinity CO2 uptake in Synechococcus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol Microbiol 32: 1305–1315

Krubasik P and Sandmann G (2000) A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol Gen Genet 263: 423–432

La Roche J, Van der Staay GW, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrench PM, Larkum AW and Green BR (1996) Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93: 15244–15248

Lewin RA (1976) Prochlorophyta as a proposed new division of algae. Nature 261: 697–698

Lewin RA and Withers NW (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256: 735–737

Li WKW (1995) Composition of ultraphytoplankton in the central North Atlantic. Mar Ecol Prog Ser 122: 1–8

Lindahl M, Funk C, Webster J, Bingsmark S, Adamska I and Andersson B (1997) Expression of ELIPs and PS II-S protein in spinach during acclimative reduction of the Photosystem II antenna in response to increased light intensities. Photosynth Res 54: 227–236

Linden H, Misawa N, Saito T and Sandmann G (1994) A novel carotenoid biosynthesis gene coding for zeta-carotene desaturase: functional expression, sequence and phylogenetic origin. Plant Mol Biol 24: 369–379

Liu H, Nolla HA and Campbell L (1997) Prochlorococcus growth rate and contribution to primary production in the Equatorial and Subtropical North Pacific Ocean. Aquat Microb Ecol 12: 39–47

Lockhardt PJ, Penny D, Hendy MD and Larkum ADW (1993) Is Prochlorothrix hollandica the best choice as a prokaryotic model for higher plant Chl a/b photosynthesis? Photosynth Res 37: 61–68

Lokstein H, Steglich C and Hess WR (1999) Light-harvesting antenna function of phycoerythrin in Prochlorococcus marinus. Biochim Biophys Acta 1410: 97–98

Maid U, Valentin K and Zetsche K (1990) The psbA-gene from a red alga resembles those from cyanobacteria and cyanelles. Curr Genet 17: 255–259

Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Stredwick JM, Garrity GM, Li B, Olsen GJ, Pramanik S, Schmidt TM and Tiedje JM (2000) The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28: 173–174

Mann EL (2000) Trace metals and the ecology of marine cyanobacteria. PhD Thesis, MIT and WHOI

Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P and Atlas R (2001) An overview of the genome of Nostoc punc tiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70: 85–106 (this issue)

Meyer G and Kloppstech K (1984) A rapidly light-induced chloroplast protein with a high turnover coded for by pea nuclear DNA. Eur J Biochem 138: 201–207

Moore LR and Chisholm SW(1999) Photophysiology of theMarine CyanobacteriumProchlorococcus: Ecotypic differences among cultured isolates. Limnol Oceanogr 44: 628–638

Moore LR, Goericke R and Chisholm SW (1995)Comparative physiology of Synechococcus and Prochlorococcus: Influence of light and temperature on on growth, pigments, fluorescence and absorptive properties. Mar Ecol Prog Ser 116: 259–275

Moore LR, Rocap G and Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467

Morden CW and Golden SS (1989) psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385

Morel A, Ahn YW, Partensky F, Vaulot D and Claustre H (1993) Prochlorococcus and Synechococcus: A comparative study of their size, pigmentation and related optical properties. J Mar Res 51: 617–649

Niyogi KK, Bjorkman O and Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94: 14162–14167

Niyogi KK, Grossman AR and Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121–1134

Omata T, Price GD, Badger MR, Okamura M, Gohta S and Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96: 13571–13576

Ong LJ and Glazer AN (1991) Phycoerythrins of marine unicellular cyanobacteria. I. Bilin types and locations and energy transfer pathways in Synechococcus spp. phycoerythrins. J Biol Chem 266: 9515–9527

Öquist G, Campbell D, Clarke AK and Gustafsson P (1995) The cyanobacterium Synechococcus modulates Photosystem II function in response to excitation stress through D1 exchange. Photosynth Res 46: 151–158

Oster U, Tanaka R, Tanaka A and Rudiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21: 305–310

Palenik B and Haselkorn R (1992) Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355: 265–267

Partensky F, Blanchot J and Vaulot D (1999a) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: A review. In: Charpy L and Larkum AWD(eds) Marine Cyanobacteria, Vol 19, pp 457–475. Musée Océanographique, Monaco

Partensky F, Hess WR and Vaulot D (1999b) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106–127

Penno S, Campbell L and Hess WR (2000) Presence of phycoerythrin in two strains of Prochlorococcus isolated from the sub-tropical North Pacific Ocean. J Phycol 36: 723- 729

Pichard SL, Campbell L and Paul JH (1997) Diversity of the ribulose bisphosphate carboxylase/oxygenase form I gene (rbcL) in natural phytoplankton communities. Appl Environ Microbiol 63: 3600–3606

Potter E and Kloppstech K (1993) Effects of light stress on the expression of early light-inducible proteins in barley. Eur J Biochem 214: 779–786

Price GD, Coleman JR and Badger MR (1992) Association of carbonic anhydrase with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100: 784–793

Raven JA (1997a) Putting the C in phycology. Eur J Phycol 32: 319–333

Raven JA (1997b) The role of marine biota in the evolution of terrestrial biota: Gases and genes. Biogeochemistry 39: 139–164

Reith ME and Munholland J (1995) Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol Biol Rep 13: 333–335

Richaud C and Zabulon G (1997) The heme oxygenase gene (pbsA) in the red alga Rhodella violacea is discontinuous and transcriptionally activated during iron limitation. Proc Natl Acad Sci USA 94: 11736–11741

Rippka R, Coursin T, Hess WR, Lichtlé C, Scanlan DJ, Palinska K, Iteman I, Partensky F, Houmard J and Herdman M (2000) Prochlorococcus marinus Chisholm et al. (1992), subsp. nov. pastoris, strain PCC 9511, the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria). Internat J Syst Env Microbiol 50: 1833–1847

Rocap G (2000) Genetic diversity and ecotypic differentiation in the marine cyanobacteria Prochlorococcus and Synechococcus. PhD Thesis, MIT and WHOI

Rocap G, Moore LR and Chishom SW (1999) Molecular phylogeny of Prochlorococcus ecotypes In: Charpy L and Larkum AWD (eds) Marine Cyanobacteria, pp 107–116. Bulletin de l'Institut Océanographique, Monaco, Special Issue No 19, 632 pp

Sandmann G (1994) Carotenoid biosynthesis inmicroorganisms and plants. Eur J Biochem 223: 7–24

Schmitz O, Katayama M, Williams SB, Kondo T and Golden SS (2000) CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science289: 765–768.

Schyns G, Rippka R, Namane A, Campbell D, Herdman M and Houmard J (1997) Prochlorothrix hollandica PCC 9006: Genomic properties of an axenic representative of the chlorophyll a/b-containing oxyphotobacteria. Res Microbiol 148: 345–354

Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A and Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: Novel genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98: 11789–11794

Shimada A, Kanai S and Maruyama T (1995) Partial sequence of ribulose-1,5-bisphosphate carboxylase/oxygenase and the phylogeny of Prochloron and Prochlorococcus (Prochlorales). J Mol Evol 40: 671–677

Shively JM, Bradburne CE, Aldrich HC, Bobik AC and Mehlman JL (1998a) Sequence homologs of the carboxysomal polypeptide CsoS1 of the Thiobacilli are present in cyanobacteria and enteric bacteria that form carboxysomes/polyhedral bodies. Can J Bot 76: 906–916

Shively JM, van Keulen G and Mejer WM (1998b) Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu Rev Microbiol 52: 191–230

Smith KS and Ferry 6JG (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24: 335–366

So AKC and Espie GS (1998) Cloning, characterization and expression of carbonic anhydrase from the cyanobacterium Synechocystis PCC 6803. Plant Mol Biol 37: 205–215

Soitamo AJ, Zhou G, Clarke AK, Öquist G, Gustafsson P and Aro EM (1996) Over-production of the D1:2 protein makes Syne chococcus cells more tolerant to photoinhibition of Photosystem II. Plant Mol Biol 30: 467–478

Steglich C, Behrenfeld M, Koblizek M, Claustre H, Penno S, Prasil O, Partensky F and Hess WR (2001) Nitrogen deprivation strongly affects Photosystem II but not phycoerythrin level in the divinyl-chlorophyll b-containing cyanobacterium Prochlorococcus marinus. Biochim Biophys Acta 1503: 341–349

Stirewalt VL, Michalowski CB, Löffelhardt W, Bohnert HJ and Bryant DA (1995) Nucleotide sequence of the cyanelle genome from Cyanophora paradoxa. Plant Mol Biol Rep 13: 327–332

Strehl B, Holtzendorff J, Partensky F and Hess WR (1999) A small and compact genome in the marine cyanobacterium Prochlorococcus marinus CCMP 1375: Lack of an intron in the gene for tRNA(Leu)UAA and a single copy of the rRNA operon. FEMS Microbiol Lett 181: 261–266

Swofford DL (2000) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer Associates, Sunderland, Massachusetts

Tabita FR (1999) Microbial ribulose1,5-bisphosphate carboxylase/-xygenase: A different perspective. Photosynth Res 60: 1–28

Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K and Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95: 12719–12723

Tchernov D, Helman Y, Keren N, Luz B, Ohad I, Reinhold L, Ogawa T and Kaplan A (2001) Passive entry of CO2 and its energy-dependent intracellular conversion to HCO3 in cyanobacteria are driven by a Photosystem I-generated delta µH+. J Biol Chem 276: 23450–23455

Ting C, Rocap G, King J and Chisholm SW (1999) Characterization of phycoerythrin genes in the chlorophyll a 2/b 2-containing prokaryote, Prochlorocccus sp. MIT9303. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, pp 225–228. Kluwer Academic Publishers, Dordrecht, The Netherlands

Ting CS, Rocap G, King J and Chisholm SW (2001) Phycobiliprotein genes of the marine photosynthetic prokaryote Prochlorococcus: Evidence for rapid evolution of genetic heterogeneity. Microbiology 147: 3171–3182

Tomitani A, Okada K, Miyashita H, Matthijs HC, Ohno T and Tanaka A (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400: 159–162

Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45: 744–750

Urbach E, Robertson DL and Chisholm SW (1992) Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355: 267–270

Urbach E, Scanlan DJ, Distel DL, Waterbury JB and Chisholm SW (1998) Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol 46: 188–201

Veldhuis MJW, Kraay GW, Van Bleijswijk JDL and Baars MA (1997) Seasonal and spatial variation in phytoplankton biomass, productivity and growth in the northwestern Indian Ocean: The southwest and northeast monsoon, 1992- 1993. Deep Sea Res 44: 425–449

Vierstra RD and Davis 6SJ (2000) Bacteriophytochromes: New tools for understanding phytochrome signal transduction. Semin Cell Dev Biol 11: 511–521

Viveiros M, Krubasik P, Sandmann G and Houssaini-Iraqui M (2000) Structural and functional analysis of the gene cluster encoding carotenoid biosynthesis in Mycobacterium aurum A+. FEMS Microbiol Lett 187: 95–101

Vrba JM and Curtis SE (1989) Characterization of a four-member psbA gene family from the cyanobacterium Anabaena PCC 7120. Plant Mol Biol 14: 81–92

Watson GM and Tabita FR (1996) Regulation, unique gene organization and unusual primary structure of carbon fixation genes from a marine phycoerythrin-containing cyanobacterium. Plant Mol Biol 32: 1103–1115

Wilbanks SM and Glazer AN (1993) Rod structure of a phycoerythrin II-containing phycobilisome. I. Organization and sequence of the gene cluster encoding the major phycobiliprotein rod components in the genome of marine Synechococcus sp. WH8020. J Biol Chem 268: 1226–1235

Williams JGK and Chisholm DA (1987) Nucleotide sequences of both psbD genes from the cyanobacterium Synechocystis PCC 6803. In: Biggins J (ed) Progress in Photosynthesis Research, pp 809–812. Martinus Nijhoff, Dordrecht, The Netherlands

Willows RD, Mayer SM, Foulk MS, DeLong A, Hanson K, Chory J and Beale SI (2000) Phytobilin biosynthesis: The Synechocystis sp. PCC 6803 heme oxygenase-encoding ho1 gene complements a phytochrome-deficient Arabidopsis thaliana hy1 mutant. Plant Mol Biol 113–120

Yoshihara S, Suzuki F, Fujita H, Geng XX and Ikeuchi M (2000) Novel putative photoreceptor and regulatory genes required for the positive phototactic movement of the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 41: 1299–1304