Subcellular localization and clues for the function of the HetN factor influencing heterocyst distribution in Anabaena sp. strain PCC 7120

Journal of Bacteriology

Volumn 196, Issue 19, 2014, Pages 3452-3460

  Corrales Guerrero, Laura ^a   Mariscal, Vicente ^a   Nu¨rnberg, Dennis J ^b   Elhai, Jeff ^c   Mullineaux, Conrad W ^b   Flores, Enrique ^a   Herrero, Antonia ^a  

^a CSIC   (Spain)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN HETN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; HETN PROTEIN, ANABAENA; OXIDOREDUCTASE;

AMINO ACID SEQUENCE; ANABAENA; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; FLUORESCENCE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; THYLAKOID MEMBRANE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRACELLULAR SPACE; METABOLISM; MOLECULAR GENETICS; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANABAENA; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; INTRACELLULAR SPACE; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

EID: 84907017792     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01922-14     Document Type: Article

References (35)

1. Flores E, Herrero A. 2010. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat. Rev. Microbiol. 8:39-50. http://dx.doi.org/10.1038/nrmicro2242.
2. Kumar K, Mella-Herrera RA, Golden JW. 2010. Cyanobacterial heterocysts. Cold Spring Harb. Perspect. Biol. 2:a000315. http://dx.doi.org/10.1101/cshperspect.a000315.
3. Herrero A, Picossi S, Flores E. 2013. Gene expression during heterocyst differentiation. Adv. Bot. Res. 65:281-329. http://dx.doi.org/10.1016/B978-0-12-394313-2.00008-1.
4. Yoon HS, Golden JW. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935-938. http://dx.doi.org/10.1126/science.282.5390.935.
5. Zhang W, Du Y, Khudyakov I, Fan Q, Gao H, Ning D, Wolk P, Xu X. 2007. A cluster that regulates both heterocyst differentiation and pattern formation in Anabaena sp. strain PCC 7120. Mol. Microbiol. 66:1429- 1443. http://dx.doi.org/10.1111/j.1365-2958.2007.05997.x.
6. Wong FC, Meeks JC. 2001. The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J. Bacteriol. 183:2654-2661. http://dx.doi.org/10.1128/JB.183.8.2654-2661.2001.
7. Risser DD, Callahan SM. 2008. HetF and PatA control levels of HetR in Anabaena sp. strain PCC 7120. J. Bacteriol. 190:7645-7654. http://dx.doi.org/10.1128/JB.01110-08.
8. Liang J, Scarpino 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. Natl. Acad. Sci. U. S. A. 89:5655-5659. http://dx.doi.org/10.1073/pnas.89.12.5655.
9. - mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. J. Bacteriol. 176:2282-2292.
10. Callahan SM, Buikema WJ. 2001. The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120. Mol. Microbiol. 40:941- 950. http://dx.doi.org/10.1046/j.1365-2958.2001.02437.x.
11. Corrales-Guerrero L, Mariscal V, Flores E, Herrero A. 2013. Functional dissection and evidence for intercellular transfer of the heterocystdifferentiation PatS morphogen. Mol. Microbiol. 88:1093-1105. http://dx.doi.org/10.1111/mmi.12244.
12. Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M, Tabata S. 2001. Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8:205-213. http://dx.doi.org/10.1093/dnares/8.5.205.
13. Bauer CC, Ramaswamy KS, Endley S, Scappino LA, Golden JW, Haselkorn R. 1997. Suppression of heterocyst differentiation in Anabaena PCC 7120 by a cosmid carrying wild-type genes encoding enzymes for fatty acid biosynthesis. FEMS Microbiol. Lett. 151:23-30. http://dx.doi.org/10.1111/j.1574-6968.1997.tb10390.x.
14. Higa KC, Rajagopalan R, Risser DD, Rivers OS, Tom SK, Videau P, Callahan SM. 2012. The RGSGR amino acid motif of the intercellular signaling protein, HetN, is required for patterning of heterocysts in Anabaena sp. strain PCC 7120. Mol. Microbiol. 83:682-693. http://dx.doi.org/10.1111/j.1365-2958.2011.07949.x.
15. Liu J, Chen W-L. 2009. Characterization of HetN, a protein involved in heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. FEMS Microbiol. Lett. 297:17-23. http://dx.doi.org/10.1111/j.1574 -6968.2009.01644.x.
16. Lo´pez-Igual R, Picossi S, Lo´pez-Garrido J, Flores E, Herrero A. 2012. N and C control of ABC-type bicarbonate transporter Cmp and its LysRtype transcriptional regulator CmpR in a heterocyst-forming cyanobacterium, Anabaena sp. Environ. Microbiol. 14:1035-1048. http://dx.doi.org/10.1111/j.1462-2920.2011.02683.x.
17. Black TA, Cai Y, Wolk CP. 1993. Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol. Microbiol. 9:77-84. http://dx.doi.org/10.1111/j.1365 -2958.1993.tb01670.x.
18. Valladares A, Rodri´guez V, Camargo S, Marti´nez-No¨el GMA, Herrero A, Luque I. 2011. Specific role of the cyanobacterial PipX factor in heterocysts of Anabaena sp. strain PCC 7120. J. Bacteriol. 193:1172-1182. http://dx.doi.org/10.1128/JB.01202-10.
19. Elhai J, Vepritskiy A, Muro-Pastor AM, Flores E, Wolk CP. 1997. Reduction of conjugal transfer efficiency by three restriction activities of Anabaena sp. strain PCC 7120. J. Bacteriol. 179:1998-2005.
20. Cai Y, Wolk CP. 1990. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J. Bacteriol. 172:3138-3145.
21. Elhai J, Taton A, Massar J, Myers JK, Travers M, Casey J, Slupesky M, Shrager J. 2009. BioBIKE: a Web-based, programmable, integrated biological knowledge base. Nucleic Acids Res. 37:W28-W32. http://dx.doi.org/10.1093/nar/gkp354.
22. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
23. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673.
24. Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics 20:426-427. http://dx.doi.org/10.1093/bioinformatics/btg430.
25. Felsenstein J. 2005. PHYLIP (phylogeny inference package), version 3.6. Department of Genome Sciences, University of Washington, Seattle, WA.
26. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40:D302-D305. http://dx.doi.org/10.1093/nar/gkr931.
27. Li B, Huang X, Zhao J. 2002. Expression of hetN during heterocyst differentiation and its inhibition of hetR up-regulation in the cyanobacterium Anabaena sp. PCC 7120. FEBS Lett. 517:87-91. http://dx.doi.org/10.1016/S0014-5793(02)02582-6.
28. Dinh T, Bernhardt TG. 2011. Using superfolder green fluorescent protein for periplasmic protein localization studies. J. Bacteriol. 193:4984-4987. http://dx.doi.org/10.1128/JB.00315-11.
29. Dammeyer T, Tinnefeld P. 2012. Engineered fluorescent proteins illuminate the bacterial periplasm. Comput. Struct. Biotechnol. J. 3:e201210013. http://dx.doi.org/10.5936/csbj.201210013.
30. Fan Q, Huang G, Lechno-Yossef S, Wolk CP, Kaneko T, Tabata S. 2005. Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120. Mol. Microbiol. 58:227-243. http://dx.doi.org/10.1111/j.1365-2958.2005.04818.x.
31. Murry MA, Olafsen AG, Benemann JR. 1981. Oxidation of diaminobenzidine in the heterocysts of Anabaena cylindrica. Curr. Microbiol. 6:201- 206. http://dx.doi.org/10.1007/BF01566972.
32. Kumazaki S, Akari M, Hasegawa M. 2013. Transformation of thylakoid membranes during differentiation from vegetative cell into heterocyst visualized by microscopic spectral imaging. Plant Physiol. 161:1321-1333. http://dx.doi.org/10.1104/pp.112.206680.
33. Chang B, Halgamuge S, Tang S-L. 2006. Analysis of SD sequences in completed microbial genomes: non-SD-led genes are as common as SDled genes. Gene 373:90-99. http://dx.doi.org/10.1016/j.gene.2006.01.033.
34. Mariscal V, Herrero A, Flores E. 2007. Continuous periplasm in a filamentous, heterocyst-forming cyanobacterium. Mol. Microbiol. 65:1139- 1145. http://dx.doi.org/10.1111/j.1365-2958.2007.05856.x.
35. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, Tandeau de Marsac N, Rippka R, Herdman M, Sivonen K, Coursin T, Laurent T, Goodwin L, Nolan M, Davenport KW, Han CS, Rubin EM, Eisen JA, Woyke T, Gugger M, Kerfeld CA. 2013. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. U. S. A. 110:1053-1058. http://dx.doi.org/10.1073/pnas.1217107110.