1887

Abstract

Heterocysts, cells specialized in N fixation in cyanobacteria, appeared at near to 2.1 Ga. They constitute one of the oldest forms of differentiated cells in evolution, and are thus an interesting model for studies on evolutionary-developmental biology. How heterocysts arose during evolution remains unknown. In PCC 7120, heterocyst development requires, among other genes, for the initiation of heterocyst differentiation, and , encoding a diffusible inhibitor of heterocyst formation. In this study, we report that both and are widespread among filamentous cyanobacteria that do not form heterocysts or fix N. and are found in proximity on the chromosome in several cases, such as , in which the level of HetR increased following nitrogen deprivation. The gene of could complement a mutant of PCC 7120, and of could suppress heterocyst differentiation in PCC 7120. Thus, key regulatory genes, including and , involved in heterocyst development may have evolved before heterocysts appeared, suggesting that their function was not limited to heterocyst differentiation.

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2009-05-01
2019-12-09
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References

  1. Berman-Frank, I., Lundgren, P. & Falkowski, P. ( 2003; ). Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154, 157–164.[CrossRef]
    [Google Scholar]
  2. Black, T. A., Cai, Y. & Wolk, C. P. ( 1993; ). Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol Microbiol 9, 77–84.[CrossRef]
    [Google Scholar]
  3. Borthakur, P. B., Orozco, C. C., Young-Robbins, S. S., Haselkorn, R. & Callahan, S. M. ( 2005; ). Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 57, 111–123.[CrossRef]
    [Google Scholar]
  4. Buikema, W. J. & Haselkorn, R. ( 1991; ). Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev 5, 321–330.[CrossRef]
    [Google Scholar]
  5. Buikema, W. J. & Haselkorn, R. ( 2001; ). Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc Natl Acad Sci U S A 98, 2729–2734.[CrossRef]
    [Google Scholar]
  6. Callahan, S. M. & Buikema, W. J. ( 2001; ). The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120. Mol Microbiol 40, 941–950.[CrossRef]
    [Google Scholar]
  7. Chen, H., Laurent, S., Bédu, S., Ziarelli, F., Chen, H.-L., Cheng, Y., Zhang, C.-C. & Peng, L. ( 2006; ). Studying the signaling role of 2-oxoglutaric acid using analogs that mimic the ketone and ketal forms of 2-oxoglutaric acid. Chem Biol 13, 849–856.[CrossRef]
    [Google Scholar]
  8. El-Shehawy, R., Lugomela, C., Ernst, A. & Bergman, B. ( 2003; ). Diurnal expression of hetR and diazocyte development in the filamentous non-heterocystous cyanobacterium Trichodesmium erythraeum. Microbiology 149, 1139–1146.[CrossRef]
    [Google Scholar]
  9. Goodman, C. S. & Coughlin, B. C. ( 2000; ). Introduction. The evolution of evo-devo biology. Proc Natl Acad Sci U S A 97, 4424–4425.[CrossRef]
    [Google Scholar]
  10. Herrero, A., Muro-Pastor, A. M., Valladares, A. & Flores, E. ( 2004; ). Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28, 469–487.[CrossRef]
    [Google Scholar]
  11. Honda, D., Yokota, A. & Sugiyama, J. ( 1999; ). Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48, 723–739.[CrossRef]
    [Google Scholar]
  12. Huang, X., Dong, Y. & Zhao, J. ( 2004; ). HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. Proc Natl Acad Sci U S A 101, 4848–4853.[CrossRef]
    [Google Scholar]
  13. Janson, S., Matveyev, A. & Bergman, B. ( 1998; ). The presence and expression of hetR in the non-heterocystous cyanobacterium Symploca PCC 8002. FEMS Microbiol Lett 168, 173–179.[CrossRef]
    [Google Scholar]
  14. Kimura, M. ( 1980; ). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16, 111–120.[CrossRef]
    [Google Scholar]
  15. Kuhn, I., Peng, L., Bédu, S. & Zhang, C.-C. ( 2000; ). Developmental regulation of the cell division protein FtsZ in Anabaena sp. strain PCC 7120, a cyanobacterium capable of terminal differentiation. J Bacteriol 182, 4640–4643.[CrossRef]
    [Google Scholar]
  16. Laurent, S., Chen, H., Bédu, S., Ziarelli, F., Peng, L. & Zhang, C.-C. ( 2005; ). Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 102, 9907–9912.[CrossRef]
    [Google Scholar]
  17. Li, J.-H., Laurent, S., Konde, V., Bédu, S. & Zhang, C.-C. ( 2003; ). An increase in the level of 2-oxoglutarate promotes heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Microbiology 149, 3257–3263.[CrossRef]
    [Google Scholar]
  18. Meeks, J. C. & Elhai, J. ( 2002; ). Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66, 94–121.[CrossRef]
    [Google Scholar]
  19. Mes, T. H. & Stal, L. J. ( 2005; ). Variable selection pressures across lineages in Trichodesmium and related cyanobacteria based on the heterocyst differentiation protein gene hetR. Gene 346, 163–171.[CrossRef]
    [Google Scholar]
  20. Nei, M. & Kumar, S. ( 2000; ). Molecular Evolution and Phylogenetics. New York: Oxford University Press.
  21. Palenik, B. ( 2001; ). Chromatic adaptation in marine Synechococcus atrains. Appl Environ Microbiol 67, 991–994.[CrossRef]
    [Google Scholar]
  22. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. ( 1979; ). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111, 1–61.[CrossRef]
    [Google Scholar]
  23. Risser, D. D. & Callahan, S. M. ( 2007; ). Mutagenesis of hetR reveals amino acids necessary for HetR function in the heterocystous cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189, 2460–2467.[CrossRef]
    [Google Scholar]
  24. Rzhetsky, A. & Nei, M. ( 1992; ). A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9, 945–967.
    [Google Scholar]
  25. Sakr, S., Jeanjean, R., Zhang, C.-C. & Arcondéguy, T. ( 2006; ). Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol 188, 1396–1404.[CrossRef]
    [Google Scholar]
  26. Scanlan, D. J. & West, N. J. ( 2002; ). Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 40, 1–12.[CrossRef]
    [Google Scholar]
  27. Stal, L. J. & Krumbein, W. E. ( 1981; ). Aerobic nitrogen fixation in pure cultures of a benthic marine Oscillatoria (cyanobacteria). FEMS Microbiol Lett 11, 295–298.[CrossRef]
    [Google Scholar]
  28. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  29. Tomitani, A., Knoll, A. H., Cavanaugh, C. M. & Ohno, T. ( 2006; ). The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci U S A 103, 5442–5447.[CrossRef]
    [Google Scholar]
  30. Webb, E. A., Moffett, J. W. & Waterbury, J. B. ( 2001; ). Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): identification of the IdiA protein. Appl Environ Microbiol 67, 5444–5452.[CrossRef]
    [Google Scholar]
  31. Wilmotte, A. & Herdmann, M. ( 2001; ). Phylogenetic relationships among the cyanobacteria based on 16S rDNA sequences. In Bergey's Manual of Systematic Bacteriology, vol. 1, pp. 487–493. Edited by D. R. Boone & R.W. Castenholz. New York: Springer.
  32. Wolk, C. P., Cai, Y., Cardemil, L., Flores, E., Hohn, R., Murry, M., Schmetterer, G., Schrautemeier, B. & Wilson, R. ( 1988; ). Isolation and complementation of mutants of Anabaena sp. strain PCC 7120 unable to grow aerobically on dinitrogen. J Bacteriol 170, 1239–1244.
    [Google Scholar]
  33. Wolk, C. P., Ernst, A. & Elhai, J. ( 1994; ). Heterocyst metabolism and development. In The Molecular Biology of Cyanobacteria, 2nd edn, pp. 769–823. Edited by D. A. Bryant. Dordrecht, The Netherlands: Kluwer.
  34. Yamaoka, T., Satoh, K. & Katoh, S. ( 1978; ). Photosynthetic activities of a thermophilic blue-green alga. Plant Cell Physiol 19, 943–954.
    [Google Scholar]
  35. Yoon, H. S. & Golden, J. W. ( 1998; ). Heterocyst pattern formation controlled by a diffusible peptide. Science 282, 935–938.[CrossRef]
    [Google Scholar]
  36. Zehr, J. P., Carpenter, E. J. & Villareal, T. A. ( 2000; ). New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. Trends Microbiol 8, 68–73.[CrossRef]
    [Google Scholar]
  37. Zhang, C.-C., Laurent, S., Sakr, S., Peng, L. & Bédu, S. ( 2006a; ). Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59, 367–375.[CrossRef]
    [Google Scholar]
  38. Zhang, J.-Y., Zou, J., Bao, Q., Chen, W.-L., Wang, L., Yang, H. & Zhang, C.-C. ( 2006b; ). A lithium-sensitive and sodium-tolerant 3′-phosphoadenosine-5′-phosphatase encoded by halA from the cyanobacterium Arthrospira platensis is closely related to its counterparts from yeasts and plants. Appl Environ Microbiol 72, 245–251.[CrossRef]
    [Google Scholar]
  39. Zhou, R., Cao, Z. & Zhao, J. ( 1998a; ). Characterization of HetR protein turnover in Anabaena sp. PCC 7120. Arch Microbiol 169, 417–423.[CrossRef]
    [Google Scholar]
  40. Zhou, R., Wei, X., Jiang, N., Li, H., Dong, Y., Hsi, K. L. & Zhao, J. ( 1998b; ). Evidence that HetR protein is an unusual serine-type protease. Proc Natl Acad Sci U S A 95, 4959–4963.[CrossRef]
    [Google Scholar]
  41. Zuckerkandl, E. & Pauling, L. ( 1965; ). Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins, pp. 97–166. Edited by V. Bryson & H. J. Vogel. New York: Academic Press.
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