 denotes the mean square; * Significant difference.
GeneBank Accession No., gene locus tag and putative protein length of PatAL and HetF cyanobacterial homologs used for phylogenetic analysis. Information on proteins used for phylogenetic analysis of PatAL and HetF Canonical PatAL and HetF sequences in Anabaena sp. PCC 7120 used as queries in BLASTP searches are highlighted green and Cylindrospermopsis raciborskii CS-505 and Raphidiopsis brookii D9 are highlighted in magenta.
Nucleotide sequences of primers used in this study. Primer names, sequence and target locus tag in C. raciborskii are shown (gene name is given in parentheses).
The authors would like to thank S. Lindwall (Stockholm University) for her invaluable support and technical advice regarding immune-TEM analysis.
Conceived and designed the experiments: MV AMP BB. Performed the experiments: AMP JL ND IO. Analyzed the data: AMP JL MV BB. Contributed reagents/materials/analysis tools: AMP MV BB JL. Wrote the paper: AMP MV BB JL.
1. Bergman B, Gallon J, Rai AN, Stal L (1997) N2 fixation in non-heterocystous cyanobacteria. FEMS Microbiol Rev 19: 139–185.
3. Wilcox M, Mitchison GJ, Smith RJ (1973) Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms. J Cell Sci 12: 707–23.
4. Popa R, Weber PK, Pett-Ridge J, Finzi JA, Fallon SJ, et al. (2007) Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME J 1: 354–360.
5. Elhai J, Wolk CP (1990) Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. EMBO J 9: 3379–3388.
6. Thiel T, Lyons EM, Erker JC, Ernst A (1995) A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Nat Acad Sci (USA) 92: 9358–9362.
7. Reddy PM, Talpasayi ERS (1974) Heterocyst formation in a blue-green alga, Cylindrospermum. Nature 249: 493–494.
8. Singh PK (1976) Growth and nitrogen fixation of mutants defective in heterocyst differentiation in the blue-green alga Cylindrospermum sp. Z Allg Mikrobiol 16: 453–463.
9. Van de Water S, Simon RD (1984) Heterocyst differentiation in Cylindrospermum licheniforme: studies on the role of transcription. J Gen Microbiol 130: 789–796.
10. Liang J, Scappino L, Haselkorn R (1992) The patA gene product, which contains a region similar to CheY of Escherichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120. Proc Nat Acad Sci (USA) 89: 5655–5659.
11. Buikema WJ, Haselkorn R (2001) Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc Nat Acad Sci USA 98: 2729–2734.
12. Stucken K, John U, Cembella A, Murillo AA, Soto-Liebe K, et al. (2010) The smallest known genomes of multicellular and toxic cyanobacteria: comparison, minimal gene sets for linked traits and the evolutionary implications. PLoS One 5: e9235.
13. Padisak J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv Hydrobiol 107: 563–593.
14. Neilan BA, Saker ML, Fastner J, Torokné A, Burns BP (2003) Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Mol Ecology 12: 133–140.
15. Moisander PH, Cheshire LA, Braddy J, Calandrino ES, Hoffman M, et al. (2012) Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiol Ecol 79: 800–811.
18. Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzini Y, Kaplan A (2010) Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20: 1557–1561.
19. Neunuebel MR, Golden JW (2008) The Anabaena sp. strain PCC 7120 gene all2874 encodes a diguanylate cyclase and is required for normal heterocyst development under high-light growth conditions. J Bacteriol 190: 6829–6836.
20. Fiedler G, Arnold M, Hannus S, Maldener I (1998) The DevBCA exporter is essential for envelope formation in heterocysts of the cyanobacterium Anabaena sp. strain PCC 7120. Mol Microbiol 27: 1193–202.
22. Klint J, Rasmussen U, Bergman B (2007) FtsZ may have dual roles in the filamentous cyanobacterium Nostoc/Anabaena sp. strain PCC 7120. J Plant Physiol 164: 11–18.
24. Sandh G, Xu L, Ran L, Sundqvist G, Bulone V, et al. (2011) Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes. Proteomics 11: 406–419.
25. Sandh G, Xu L, Bergman B (2012) Diazocyte development in the marine diazotrophic cyanobacterium Trichodesmium. Microbiol 158: 345–352.
26. Wei TF, Ramasubramanian TS, Golden JW (1994) Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176: 4473–4482.
27. Olmedo-Verd E, Muro-Pastor AM, Flores E, Herrero A (2006) Localized induction of the ntcA regulatory gene in developing heterocysts of Anabaena sp. strain PCC 7120. J Bacteriol 188: 6694–6699.
28. Thiel T, Pratte B (2001) Effect on heterocyst differentiation of nitrogen fixation in vegetative cells of the cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 183: 280–286.
29. Liu J, Wolk CP (2011) Genes patA and patL of Anabaena sp. strain PCC 7120 have similar mutant phenotypes, and their products may interact. J Bacteriol 2011 193: 6070–6074.
30. Risser DD, Callahan SM (2008) HetF and PatA control levels of HetR in Anabaena sp. strain PCC 7120. J Bacteriol 190: 7645–7654.
31. Makarova KS, Koonin EV, Haselkorn R, Galperin MY (2006) Cyanobacterial response regulator PatA contains a conserved N-terminal domain (PATAN) with an alpha-helical insertion. Bioinformatics 22: 1297–1301.
33. Wiedner C, Rücker J, Brüggemann R, Nixdorf B (2007) Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152: 473–84.
34. Skuja H (1938) Comments on fresh-water rhodophyceae. Bot Rev 4: 665–676.
35. Krienitz L, Hegewald E (1996) Über das Vorkommen von wärmeliebenden Blaualgenarten in einem norddeutschen Gewässer. Lauterbornia H 26: 55–63.
36. Rücker J, Wiedner C, Zippel P (1997) Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes. Hydrobiol 342/343: 107–115.
37. Dokulil MT, Mayer J (1996) Population dynamics and photosynthetic rates of a Cylindrospermopsis-Limnothrix association in a highly eutrophic urban lake, Alte Donau, Vienna, Austria. Algol Stud 83: 179–195.
38. Couté A, Leitao M, Martin C (1997) Premiere observation du genre Cylindrospermopsis (Cyanophyceae, Nostocales) en France. Cryptogram Algol 18: 57–70.
39. Saker ML, Nogueira ICG, Vasconcelos VM, Neilan BA, Eaglesham GK, et al. (2003