Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Park, Jeong Jin ^a,b,d   Lechno Yossef, Sigal ^a   Wolk, Coleman P ^a   Vieille, Claire ^a,b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Washington State University ^*  (United States)

^c Michigan State University   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Amino acid biosynthesis; Anabaena variabilis; Heterocyst; Microarray; Transcript levels; Vegetative cell

Indexed keywords

CARBON DIOXIDE; CARRIER PROTEIN; FRUCTOSE; GLUTAMIC ACID; GLUTAMINE; GLYCINE; PROLINE; SERINE; SUCROSE; THREONINE;

AMINO ACID SYNTHESIS; ANABAENA VARIABILIS; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; CELL CULTURE; CELL SPECIFICITY; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; HETEROTROPHY; MIXOTROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PHOTOTROPHY; PHYCOBILISOME; UPREGULATION; VEGETATIVE GROWTH;

ANABAENA; ANABAENA VARIABILIS;

AMINO ACIDS; ANABAENA VARIABILIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROTROPHIC PROCESSES; NITROGEN FIXATION; PHOTOTROPHIC PROCESSES; TISSUE ARRAY ANALYSIS;

EID: 84887038040     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-759     Document Type: Article

References (110)

1. Thiel T. Genetic analysis of cyanobacteria. The Molecular Biology of Cyanobacteria 1994, 581-611. Dordrecht, NL: Kluwer Academic Publishers, Bryant DA.
2. Peterson RB, Wolk CP. High recovery of nitrogenase activity and of 55Fe-labeled nitrogenase in heterocysts isolated from Anabaena variabilis. Proc Natl Acad Sci U S A 1978, 75:6271-6275. 10.1073/pnas.75.12.6271, 393163, 16592599.
3. Thiel T, Pratte BS. Effect on heterocyst differentiation of nitrogen fixation in vegetative cells of the cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 2001, 183:280-286. 10.1128/JB.183.1.280-286.2001, 94876, 11114927.
4. Wolk CP, Ernst A, Elhai J. Heterocyst metabolism and development. The Molecular Biology of Cyanobacteria 1994, 769-823. Dordrecht: Kluwer Academic Publishers, Bryant DA.
5. Walsby AE. Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends Microbiol 2007, 15:340-349. 10.1016/j.tim.2007.06.007, 17644394.
6. Thomas J, Meeks JC, Wolk CP, Shaffer PW, Austin SM. Formation of glutamine from 13N-ammonia, 13N-dinitrogen, and 14C-glutamate by heterocysts isolated from Anabaena cylindrica. J Bacteriol 1977, 129:1545-1555. 235134, 14927.
7. Martín-Figueroa E, Navarro F, Florencio FJ. The GS-GOGAT pathway is not operative in the heterocysts. Cloning and expression of glsF gene from the cyanobacterium Anabaena sp. PCC 7120. FEBS Lett 2000, 476:282-286. 10.1016/S0014-5793(00)01722-1, 10913629.
8. López-Igual R, Flores E, Herrero A. Inactivation of a heterocyst-specific invertase indicates a principal role of sucrose catabolism in heterocysts of Anabaena sp. J Bacteriol 2010, 192:5526-5533. 10.1128/JB.00776-10, 2950499, 20729363.
9. Vargas WA, Nishi CN, Giarrocco LE, Salerno GL. Differential roles of alkaline/neutral invertases in Nostoc sp. PCC 7120: Inv-B isoform is essential for diazotrophic growth. Planta 2011, 233:153-162. 10.1007/s00425-010-1288-5, 20938678.
10. Razquin P, Schmitz S, Peleato ML, Fillat MF, Gómez-Moreno C, Böhme H. Differential activities of heterocyst ferredoxin, vegetative cell ferredoxin, and flavodoxin as electron carriers in nitrogen fixation and photosynthesis in Anabaena sp. Photosynth Res 1995, 43:35-40.
11. Muro-Pastor MI, Reyes JC, Florencio FJ. Ammonium assimilation in cyanobacteria. Photosynth Res 2005, 83:135-150. 10.1007/s11120-004-2082-7, 16143848.
12. Thiel T. Nitrogen fixation in heterocyst-forming cyanobacteria. Genetics and Regulation of Nitrogen Fixation in Free-Living Bacteria 2004, 73-110. Dordrecht: Kluwer Academic Publishers, Klipp W, Masepohl B, Gallon JR, Newton WE.
13. Nicolaisen K, Hahn A, Schleiff E. The cell wall in heterocyst formation by Anabaena sp. PCC 7120. J Basic Microbiol 2009, 49:5-24. 10.1002/jobm.200800300, 19253332.
14. Kumar K, Mella-Herrera RA, Golden JW. Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2009, 2:a000315.
15. Flores E, Herrero A. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 2010, 8:39-50. 10.1038/nrmicro2242, 19966815.
16. Zhao J, Wolk CP. Developmental biology of heterocysts, 2006. Myxobacteria: Multicellularity and Differentiation 2008, 397-418. Washington D. C: ASM Press, Whitworth DE.
17. Xu X, Elhai J, Wolk CP. Transcriptional and developmental responses by Anabaena to deprivation of fixed nitrogen. The Cyanobacteria: Molecular Biology, Genomics and Evolution 2008, 383-422. Norwich, U.K: Caister Academic Press, Herrero A, Flores E.
18. Meeks JC, Campbell EL, Summers ML, Wong FC. Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 2002, 178:395-403. 10.1007/s00203-002-0476-5, 12420158.
19. Zhang C-C, Laurent S, Sakr S, Peng L, Bédu S. Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 2006, 59:367-375. 10.1111/j.1365-2958.2005.04979.x, 16390435.
20. Ehira S, Ohmori M, Sato N. Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 2003, 10:97-113. 10.1093/dnares/10.3.97, 12886952.
21. Ehira S, Ohmori M. NrrA, a nitrogen-responsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Mol Microbiol 2006, 59:1692-1703. 10.1111/j.1365-2958.2006.05049.x, 16553876.
22. Campbell EL, Summers ML, Christman H, Martin ME, Meeks JC. Global gene expression patterns of Nostoc punctiforme in steady-state dinitrogen-grown heterocyst-containing cultures and at single time points during the differentiation of akinetes and hormogonia. J Bacteriol 2007, 189:5247-5256. 10.1128/JB.00360-07, 1951844, 17483217.
23. Kushige H, Kugenuma H, Matsuoka M, Ehira S, Ohmori M, Iwasaki H. Genome-wide and heterocyst-specific circadian gene expression in the filamentous cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 2013, 195:1276-1284. 10.1128/JB.02067-12, 3592012, 23316037.
24. Flaherty BL, Van Nieuwerburgh F, Head SR, Golden JW. Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp. strain PCC 7120 to combined-nitrogen deprivation. BMC Genomics 2011, 12:332. 10.1186/1471-2164-12-332, 3141674, 21711558.
25. Mitschke J, Vioque A, Haas F, Hess WR, Muro-Pastor AM. Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc Natl Acad Sci U S A 2011, 108:20130-20135. 10.1073/pnas.1112724108, 3250118, 22135468.
26. Ow SY, Cardona T, Taton A, Magnuson A, Lindblad P, Stensjö K, Wright PC. Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. J Proteome Res 2008, 7:1615-1628. 10.1021/pr700604v, 18290607.
27. Ow SY, Noirel J, Cardona T, Taton A, Lindblad P, Stensjö K, Wright PC. Quantitative overview of N2 fixation in Nostoc punctiforme ATCC 29133 through cellular enrichments and iTRAQ shotgun proteomics. J Proteome Res 2009, 8:187-198. 10.1021/pr800285v, 19012430.
28. Cardona T, Battchikova N, Zhang P, Stensjö K, Aro E-M, Lindblad P, Magnuson A. Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochim Biophys Acta 2009, 1787:252-263. 10.1016/j.bbabio.2009.01.015, 19366613.
29. Wiechert W, Mollney M, Petersen S, de Graaf AA. A universal framework for 13C metabolic flux analysis. Metab Engin 2001, 3:265-283.
30. Ratcliffe RG, Shachar-Hill Y. Measuring multiple fluxes through plant metabolic networks. Plant J 2006, 45:490-511. 10.1111/j.1365-313X.2005.02649.x, 16441345.
31. Young JD, Shastri AA, Stephanopoulos G, Morgan JA. Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis. Metab Engin 2011, 13:656-665.
32. Wolk CP, Shaffer PW. Heterotrophic micro- and macrocultures of a nitrogen-fixing cyanobacterium. Arch Microbiol 1976, 110:145-147. 10.1007/BF00690221, 828022.
33. Haury JF, Spiller H. Fructose uptake and influence on growth of and nitrogen fixation by Anabaena variabilis. J Bacteriol 1981, 147:227-235. 216029, 6787026.
34. Stebegg R, Wurzinger B, Mikulic M, Schmetterer G. Chemoheterotrophic growth of the cyanobacterium Anabaena sp. strain PCC 7120 dependent on a functional cytochrome c oxidase. J Bacteriol 2012, 194:4601-4607. 10.1128/JB.00687-12, 3415483, 22730128.
35. Ungerer JL, Pratte BS, Thiel T. Regulation of fructose transport and its effect on fructose toxicity in Anabaena spp. J Bacteriol 2008, 190:8115-8125. 10.1128/JB.00886-08, 2593219, 18931119.
36. Hu NT, Thiel T, Giddings TH, Wolk CP. New Anabaena and Nostoc cyanophages from sewage settling ponds. Virology 1981, 114:236-246. 10.1016/0042-6822(81)90269-5, 6269286.
37. Allen MB, Arnon DI. Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Physiol 1955, 30:366-372. 10.1104/pp.30.4.366, 540664, 16654787.
38. Lechno-Yossef S, Fan Q, Ehira S, Sato N, Wolk CP. Mutations in four regulatory genes have interrelated effects on heterocyst maturation in Anabaena sp. strain PCC 7120. J Bacteriol 2006, 188:7387-7395. 10.1128/JB.00974-06, 1636280, 16936023.
39. Elhai J, Wolk CP. Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. EMBO J 1990, 9:3379-3388. 552076, 2120040.
40. Vioque A. The RNase P RNA from cyanobacteria: short tandemly repeated repetitive (STRR) sequences are present within the RNase P RNA gene in heterocyst-forming cyanobacteria. Nucleic Acids Res 1997, 25:3471-3477. 10.1093/nar/25.17.3471, 146911, 9254706.
41. Bolstad BM, Irizarry RA, Åstrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193. 10.1093/bioinformatics/19.2.185, 12538238.
42. The R Project for Statistical Computing http://www.r-project.org/.
43. Sokal RR, RohlF FJ. Biometry. The Principles and Practice of Statistics in Biological Research, 2nd edn 1981, New York: W. H. Freeman and Company.
44. Hawkinson JE, AcostaBurruel M, Wood PL. The metabotropic glutamate receptor antagonist L-2-amino-3-phosphonopropionic acid inhibits phosphoserine phosphatase. Eur J Pharmacol 1996, 307:219-225. 10.1016/0014-2999(96)00253-1, 8832224.
45. D'Angelo E, Crutchfield J, Vandiviere M. Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Quality 2001, 30:2206-2209.
46. Thiel T, Lyons EM, Erker JC, Ernst A. A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Natl Acad Sci U S A 1995, 92:9358-9362. 10.1073/pnas.92.20.9358, 40984, 7568132.
47. Golden JW, Whorff LL, Wiest DR. Independent regulation of nifHDK operon transcription and DNA rearrangement during heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 1991, 173:7098-7105. 209215, 1938911.
48. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res 2004, 32:D277-D280. 10.1093/nar/gkh063, 308797, 14681412.
49. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
50. Jensen BB, Cox RP. Effect of oxygen concentration on dark nitrogen fixation and respiration in cyanobacteria. Arch Microbiol 1983, 135:287-292.
51. Murry MA, Wolk CP. Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope. Arch Microbiol 1989, 151:469-474.
52. Valladares A, Herrero A, Pils D, Schmetterer G, Flores E. Cytochrome c oxidase genes required for nitrogenase activity and diazotrophic growth in Anabaena sp. PCC 7120. Mol Microbiol 2003, 47:1239-1249. 10.1046/j.1365-2958.2003.03372.x, 12603731.
53. Valladares A, Maldener I, Muro-Pastor AM, Flores E, Herrero A. Heterocyst development and diazotrophic metabolism in terminal respiratory oxidase mutants of the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 2007, 189:4425-4430. 10.1128/JB.00220-07, 1913370, 17416650.
54. Brusca JS, Hale MA, Carrasco CD, Golden JW. Excision of an 11-kilobase-pair DNA element from within the nifD gene in Anabaena variabilis heterocysts. J Bacteriol 1989, 171:4138-4145. 210183, 2502534.
55. Schrautemeier B, Neveling U, Schmitz S. Distinct and differently regulated Mo-dependent nitrogen-fixing systems evolved for heterocysts and vegetative cells of Anabaena variabilis ATCC 29413: characterization of the fdxH1/2 gene regions as part of the nif1/2 gene clusters. Mol Microbiol 1995, 18:357-369. 10.1111/j.1365-2958.1995.mmi_18020357.x, 8709854.
56. Thiel T. Isolation and characterization of the vnfEN genes of the cyanobacterium Anabaena variabilis. J Bacteriol 1996, 178:4493-4499. 178215, 8755876.
57. Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 2000, 28:27-30. 10.1093/nar/28.1.27, 102409, 10592173.
58. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012, 40:D109-D114. 10.1093/nar/gkr988, 3245020, 22080510.
59. Gottschalk G. Bacterial Metabolism 1986, New-York: Springer-Verlag.
60. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology Washington, DC: ASM Press, Böck A, Curtiss RIII, Kaper JB, Karp PD, Neidhardt FC, Nyström T, Slauch JM, Squires CL, Usser D, http://www.asmscience.org/content/journal/ecosalplus.
61. Wood NB, Haselkorn R. Control of phycobiliprotein proteolysis and heterocyst differentiation in Anabaena. J Bacteriol 1980, 141:1375-1385. 293836, 6767709.
62. Maldener I, Lockau W, Cai Y, Wolk CP. Calcium-dependent protease of the cyanobacterium Anabaena: molecular cloning and expression of the gene in Escherichia coli, sequencing and site-directed mutagenesis. Mol Gen Genet 1991, 225:113-120.
63. Lahmi R, Sendersky E, Perelman A, Hagemann M, Forchhammer K, Schwarz R. Alanine dehydrogenase activity is required for adequate progression of phycobilisome degradation during nitrogen starvation in Synechococcus elongatus PCC 7942. J Bacteriol 2006, 188:5258-5265. 10.1128/JB.00209-06, 1539948, 16816198.
64. Popa R, Weber PK, Pett-Ridge J, Finzi JA, Fallon SJ, Hutcheon ID, Nealson KH, Capone DG. Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME J 2007, 1:354-360.
65. Herrero A, Flores E. Transport of basic amino acids by the dinitrogen-fixing cyanobacterium Anabaena PCC 7120. J Biol Chem 1990, 265:3931-3935.
66. Montesinos ML, Herrero A, Flores E. Amino acid transport systems required for diazotrophic growth in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 1995, 177:3150-3157. 177005, 7768813.
67. Picossi S, Montesinos ML, Pernil R, Lichtle C, Herrero A, Flores E. ABC-type neutral amino acid permease N-I is required for optimal diazotrophic growth and is repressed in the heterocysts of Anabaena sp. strain PCC 7120. Mol Microbiol 2005, 57:1582-1592. 10.1111/j.1365-2958.2005.04791.x, 16135226.
68. Pernil R, Picossi S, Mariscal V, Herrero A, Flores E. ABC-type amino acid uptake transporters Bgt and N-II of Anabaena sp. strain PCC 7120 share an ATPase subunit and are expressed in vegetative cells and heterocysts. Mol Microbiol 2008, 67:1067-1080. 10.1111/j.1365-2958.2008.06107.x, 18208492.
69. Mullineaux CW, Mariscal V, Nenninger A, Khanum H, Herrero A, Flores E, Adams DG. Mechanism of intercellular molecular exchange in heterocyst-forming cyanobacteria. EMBO J 2008, 27:1299-1308. 10.1038/emboj.2008.66, 2374843, 18388860.
70. Merino-Puerto V, Schwarz H, Maldener I, Mariscal V, Mullineaux VW, Herrero A, Flores E. FraC/FraD-dependent intercellular molecular exchange in the filaments of a heterocyst-forming cyanobacterium, Anabaena sp. Mol Microbiol 2011, 82:87-98. 10.1111/j.1365-2958.2011.07797.x, 21819458.
71. Wilk L, Strauss M, Rudolf M, Nicolaisen K, Flores E, Kühlbrandt W, Schleiff E. Outer membrane continuity and septosome formation between vegetative cells in the filaments of Anabaena sp. PCC 7120. Cellular Microbiol 2011, 13:1744-1754.
72. Ernst A, Böhme H, Böger P. Phosphorylation and nitrogenase activity in isolated heterocysts from Anabaena variabilis (ATCC 29413). Biochim Biophys Acta 1983, 723:83-90.
73. Sicora CI, Appleton SE, Brown CM, Chung J, Chandler J, Cockshutt AM, Vass I, Campbell DA. Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms. Biochim Biophys Acta-Bioenergetics 2006, 1757:47-56.
74. Mulo P, Sakurai I, Aro EM. Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: From transcription to PSII repair. Biochim Biophys Acta-Bioenergetics 1817, 2012:247-257.
75. Tel-Or E, Stewart WDP. Photosynthetic components and activities of nitrogen-fixing isolated heterocysts of Anabaena cylindrica. Proc Royal Soc London B 1977, 198:61-86.
76. Thomas J. Absence of the pigments of photosystem II of photosynthesis in heterocysts of a blue-green alga. Nature 1970, 228:181-183.
77. Donze M, Haveman J, Schiereck P. Absence of photosystem 2 in heterocysts of blue-green alga Anabaena. Biochim Biophys Acta 1972, 256:157-161. 10.1016/0005-2728(72)90170-3, 4621614.
78. Black K, Osborne B. An assessment of photosynthetic downregulation in cyanobacteria from the Gunnera-Nostoc symbiosis. New Phytologist 2004, 162:125-132.
79. Enami I, Okumura A, Nagao R, Suzuki T, Iwai M, Shen JR. Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth Res 2008, 98:349-363. 10.1007/s11120-008-9343-9, 18716894.
80. Peterson RB, Dolan E, Calvert HE, Ke B. Energy transfer from phycobiliproteins to photosystem I in vegetative cells and heterocysts of Anabaena variabilis. Biochim Biophys Acta 1981, 634:237-248.
81. Johnson TR, Haynes JI, Wealand JL, Yarbrough LR, Hirschberg R. Structure and regulation of genes encoding phycocyanin and allophycocyanin from Anabaena variabilis ATCC 29413. J Bacteriol 1988, 170:1858-1865. 211042, 2450871.
82. Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nature Rev Microbiol 2008, 6:681-691.
83. Cannon GC, Heinhorst S, Kerfeld CA. Carboxysomal carbonic anhydrases: Structure and role in microbial CO2 fixation. Biochim Biophys Acta - Proteins and Proteomics 1804, 2010:382-392.
84. Peña KL, Castel SE, de Araujo C, Espie GS, Kimber MS. Structural basis of the oxidative activation of the carboxysomal γ-carbonic anhydrase, CcmM. Proc Natl Acad Sci U S A 2010, 107:2455-2460. 10.1073/pnas.0910866107, 2823891, 20133749.
85. Hagen KD, Meeks JC. The unique cyanobacterial protein OpcA is an allosteric effector of glucose-6-phosphate dehydrogenase in Nostoc punctiforme ATCC 29133. J Biol Chem 2001, 276:11477-11486. 10.1074/jbc.M010472200, 11152472.
86. Summers ML, Meeks JC. Transcriptional regulation of zwf, encoding glucose-6-phosphate dehydrogenase, from the cyanobacterium Nostoc punctiforme strain ATCC 29133. Mol Microbiol 1996, 22:473-480. 10.1046/j.1365-2958.1996.1371502.x, 8939431.
87. Winkenbach F, Wolk CP. Activities of enzymes of the oxidative and the reductive pentose phosphate pathways in heterocysts of a blue-green alga. Plant Physiol 1973, 52:480-483. 10.1104/pp.52.5.480, 366528, 16658588.
88. Valverde F, Losada M, Serrano A. Functional complementation of an Escherichia coli gap mutant supports an amphibolic role for NAD(P)-dependent glyceraldehyde-3-phosphate dehydrogenase of Synechocystis sp. strain PCC 6803. J Bacteriol 1997, 179:4513-4522. 179286, 9226260.
89. Valverde F, Peleato ML, Fillat MF, Gomez-Moreno C, Losada R, Serrano A. Simultaneous occurrence of two different glyceraldehyde-3-phosphate dehydrogenases in heterocystous N2-fixing cyanobacteria. Biochem Biophys Res Comm 2001, 283:356-363. 10.1006/bbrc.2001.4782, 11327708.
90. Schilling N, Ehrnsperger K. Cellular differentiation of sucrose metabolism in Anabaena variabilis. Z Naturforsch 1985, 40:776-779.
91. Curatti L, Giarrocco L, Salerno G. Sucrose synthase and RuBisCo expression is [sic] similarly regulated by the nitrogen source in the nitrogen-fixing cyanobacterium Anabaena sp. Planta 2006, 223:891-900. 10.1007/s00425-005-0142-7, 16261375.
92. Marcozzi C, Cumino AC, Salerno GL. Role of NtcA, a cyanobacterial global nitrogen regulator, in the regulation of sucrose metabolism gene expression in Anabaena sp. PCC 7120. Arch Microbiol 2009, 191:255-263. 10.1007/s00203-008-0450-y, 19082579.
93. Porchia AC, Salerno GL. Sucrose biosynthesis in a prokaryotic organism: presence of two sucrose-phosphate synthases in Anabaena with remarkable differences compared with the plant enzymes. Proc Natl Acad Sci U S A 1996, 93:13600-13604. 10.1073/pnas.93.24.13600, 19363, 8942980.
94. Cumino A, Ekeroth C, Salerno G. Sucrose-phosphate phosphatase from Anabaena sp. strain PCC 7120: isolation of the protein and gene revealed significant structural differences from the higher-plant enzyme. Planta 2001, 214:250-256. 10.1007/s004250100608, 11800389.
95. Cumino AC, Marcozzi C, Barreiro R, Salerno GL. Carbon cycling in Anabaena sp. PCC 7120. Sucrose synthesis in the heterocysts and possible role in nitrogen fixation. Plant Physiol 2007, 143:1385-1397. 10.1104/pp.106.091736, 1820908, 17237189.
96. Vargas W, Cumino A, Salerno GL. Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol?. Planta 2003, 216:951-960.
97. Curatti L, Flores E, Salerno G. Sucrose is involved in the diazotrophic metabolism of the heterocyst-forming cyanobacterium Anabaena sp. FEBS Lett 2002, 513:175-178. 10.1016/S0014-5793(02)02283-4, 11904145.
98. Curatti L, Giarrocco LE, Cumino AC, Salerno GL. Sucrose synthase is involved in the conversion of sucrose to polysaccharides in filamentous nitrogen-fixing cyanobacteria. Planta 2008, 228:617-625. 10.1007/s00425-008-0764-7, 18560883.
99. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci U S A 1995, 92:9353-9357. 10.1073/pnas.92.20.9353, 40983, 7568131.
100. Lang NJ, Krupp JM, Koller AL. Morphological and ultrastructural changes in vegetative cells and heterocysts of Anabaena variabilis grown with fructose. J Bacteriol 1987, 169:920-923. 211872, 3100507.
101. Huang G, Fan Q, Lechno-Yossef S, Wojciuch E, Wolk CP, Kaneko T, Tabata S. Clustered genes required for the synthesis of heterocyst envelope polysaccharide in Anabaena sp. strain PCC 7120. J Bacteriol 2005, 187:1114-1123. 10.1128/JB.187.3.1114-1123.2005, 545720, 15659688.
102. Summers ML, Wallis JG, Campbell EL, Meeks JC. Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. J Bacteriol 1995, 177:6184-6194. 177459, 7592384.
103. Wolk CP, Thomas J, Shaffer PW, Austin SM, Galonsky A. Pathway of nitrogen metabolism after fixation of 13N-labeled nitrogen gas by the cyanobacterium, Anabaena cylindrica. J Biol Chem 1976, 251:5027-5034.
104. Papen H, Neuer G, Refaian M, Bothe H. The isocitrate dehydrogenase from cyanobacteria. Arch Microbiol 1983, 134:73-79. 10.1007/BF00429411, 6409049.
105. Galmozzi CV, Saelices L, Florencio FJ, Muro-Pastor MI. Posttranscriptional regulation of glutamine synthetase in the filamentous cyanobacterium Anabaena sp. PCC 7120: differential expression between vegetative cells and heterocysts. J Bacteriol 2010, 192:4701-4711. 10.1128/JB.00222-10, 2937420, 20639319.
106. Meeks JC, Wolk CP, Thomas J, Lockau W, Shaffer PW, Austin SM, Chien WS, Galonsky A. The pathways of assimilation of 13NH4+ by the cyanobacterium, Anabaena cylindrica. J Biol Chem 1977, 252:7894-7900.
107. Chávez S, Lucena JM, Reyes JC, Florencio FJ, Candau P. The presence of glutamate dehydrogenase is a selective advantage for the cyanobacterium Synechocystis sp. strain PCC 6803 under nonexponential growth conditions. J Bacteriol 1999, 181:808-813. 93446, 9922243.
108. Ke S, Haselkorn R. The Sakaguchi reaction product quenches phycobilisome fluorescence, allowing determination of the arginine concentration in cells of Anabaena strain PCC 7120. J Bacteriol 2013, 195:25-28. 10.1128/JB.01512-12, 3536181, 23086210.
109. Prasil O, Kolber Z, Berry JA, Falkowski PG. Cyclic electron flow around photosystem II in vivo. Photosynth Res 1996, 48:395-410.
110. Long BM, Rae BD, Badger MR, Price GD. Over-expression of the beta-carboxysomal CcmM protein in Synechococcus PCC7942 reveals a tight co-regulation of carboxysomal carbonic anhydrase (CcaA) and M58 content. Photosynth Res 2011, 109:33-45. 10.1007/s11120-011-9659-8, 21597987.