1887

Abstract

Hormogonia are motile filaments produced by many filamentous cyanobacteria that function in dispersal, phototaxis and the establishment of nitrogen-fixing symbioses. The gene regulatory network promoting hormogonium development is initiated by the hybrid histidine kinase HrmK, which in turn activates a sigma factor cascade consisting of SigJ, SigC and SigF. In this study, cappable-seq was employed to define the primary transcriptome of developing hormogonia in the model filamentous cyanobacterium ATCC 29133 in both the wild-type, and , and mutant strains 6 h post-hormogonium induction. A total of 1544 transcriptional start sites (TSSs) were identified that are associated with protein-coding genes and are expressed at levels likely to lead to biologically relevant transcripts in developing hormogonia. TSS expression among the sigma-factor deletion strains was highly consistent with previously reported gene expression levels from RNAseq experiments, and support the current working model for the role of these genes in hormogonium development. Analysis of SigJ-dependent TSSs corroborated the presence of the previously identified J-Box in the −10 region of SigJ-dependent promoters. Additionally, the data presented provides new insights on sequence conservation within the −10 regions of both SigC- and SigF-dependent promoters, and demonstrates that SigJ and SigC coordinate complex co-regulation not only of hormogonium-specific genes at different loci, but within an individual operon. As progress continues on defining the hormogonium gene regulatory network, this data set will serve as a valuable resource.

Funding
This study was supported by the:
  • Division of Integrative Organismal Systems (Award 1753690)
    • Principle Award Recipient: DouglasD. Risser
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001111
2021-11-15
2021-12-03
Loading full text...

Full text loading...

References

  1. Meeks JC, Campbell EL, Summers ML, Wong FC. Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 2002; 178:395–403 [View Article] [PubMed]
    [Google Scholar]
  2. Khayatan B, Meeks JC, Risser DD. Evidence that a modified type IV pilus-like system powers gliding motility and polysaccharide secretion in Filamentous cyanobacteria. Mol Microbiol 2015; 98:1021–1036 [View Article] [PubMed]
    [Google Scholar]
  3. Risser DD, Meeks JC. Comparative transcriptomics with a motility-deficient mutant leads to identification of a novel polysaccharide secretion system in Nostoc punctiforme. Mol Microbiol 2013; 87:884–893 [View Article] [PubMed]
    [Google Scholar]
  4. Zuniga EG, Boateng KKA, Bui NU, Kurnfuli S, Muthana SM et al. Identification of a hormogonium polysaccharide-specific gene set conserved in Filamentous cyanobacteria. Mol Microbiol 2020; 114:597–608 [View Article] [PubMed]
    [Google Scholar]
  5. Castenholz RW. Motility and taxis. In Carr NG, Whitton BA. eds The Biology of Cyanobacteria Oxford: Blackwell Science; 1982 pp 413–419
    [Google Scholar]
  6. Shepard RN, Sumner DY. Undirected motility of filamentous cyanobacteria produces reticulate mats. Geobiology 2010; 8:179–190 [View Article] [PubMed]
    [Google Scholar]
  7. Tzubari Y, Magnezi L, Be’er A, Berman-Frank I. Iron and phosphorus deprivation induce sociality in the marine bloom-forming cyanobacterium Trichodesmium. ISME J 2018; 12:1682–1693 [View Article] [PubMed]
    [Google Scholar]
  8. Risser DD, Chew WG, Meeks JC. Genetic characterization of the hmp locus, a chemotaxis-like gene cluster that regulates hormogonium development and motility in Nostoc punctiforme. Mol Microbiol 2014; 92:222–233 [View Article] [PubMed]
    [Google Scholar]
  9. Pratte BS, Thiel T. Comparative genomic insights into culturable symbiotic cyanobacteria from the water fern Azolla. Microb Genom 2021; 7: [View Article] [PubMed]
    [Google Scholar]
  10. Zuniga EG, Figueroa NM, Gonzalez A, Pantoja AP, Risser DD et al. The hybrid histidine kinase HrmK is an early-acting factor in the hormogonium gene regulatory network. J Bacteriol 2020; 202:e00675-19 [View Article]
    [Google Scholar]
  11. Gonzalez A, Riley KW, Harwood TV, Zuniga EG, Risser DD. A tripartite, hierarchical sigma factor cascade promotes hormogonium development in the Filamentous cyanobacterium Nostoc punctiforme. mSphere 2019; 4:e00231-19 [View Article] [PubMed]
    [Google Scholar]
  12. 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 [View Article] [PubMed]
    [Google Scholar]
  13. Ettwiller L, Buswell J, Yigit E, Schildkraut I. A novel enrichment strategy reveals unprecedented number of novel transcription start sites at single base resolution in a model prokaryote and the gut microbiome. BMC Genomics 2016; 17:199–z199 [View Article] [PubMed]
    [Google Scholar]
  14. 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 [View Article] [PubMed]
    [Google Scholar]
  15. 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 [View Article] [PubMed]
    [Google Scholar]
  16. Splitt SD, Risser DD. The non-metabolizable sucrose analog sucralose is a potent inhibitor of hormogonium differentiation in the filamentous cyanobacterium Nostoc punctiforme. Arch Microbiol 2015; 198:137–147 [View Article]
    [Google Scholar]
  17. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002; 18:207–208 [View Article] [PubMed]
    [Google Scholar]
  18. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article] [PubMed]
    [Google Scholar]
  19. Bailey TL, Boden M, Buske FA, Frith M, Grant CE et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009; 37:W202–8 [View Article]
    [Google Scholar]
  20. Thorvaldsdóttir H, Robinson JT, Mesirov JP. tegrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013; 14:178–192 [View Article] [PubMed]
    [Google Scholar]
  21. Bell N, Lee JJ, Summers ML. Characterization and in vivo regulon determination of an ECF sigma factor and its cognate anti-sigma factor in Nostoc punctiforme. Mol Microbiol 2017; 104:179–194 [View Article] [PubMed]
    [Google Scholar]
  22. Campbell EL, Hagen KD, Chen R, Risser DD, Ferreira DP et al. Genetic analysis reveals the identity of the photoreceptor for phototaxis in hormogonium filaments of Nostoc punctiforme. J Bacteriol 2015; 197:782–791 [View Article] [PubMed]
    [Google Scholar]
  23. Campbell EL, Wong FCY, Meeks JC. DNA binding properties of the HrmR protein of Nostoc punctiforme responsible for transcriptional regulation of genes involved in the differentiation of hormogonia. Mol Microbiol 2003; 47:573–582 [View Article] [PubMed]
    [Google Scholar]
  24. Riley KW, Gonzalez A, Risser DD. A partner-switching regulatory system controls hormogonium development in the filamentous cyanobacterium Nostoc punctiforme. Mol Microbiol 2018; 109:555–569 [View Article] [PubMed]
    [Google Scholar]
  25. Asayama M, Imamura S. Stringent promoter recognition and autoregulation by the group 3 sigma-factor SigF in the cyanobacterium Synechocystis sp. strain PCC 6803. Nucleic Acids Res 2008; 36:5297–5305 [View Article] [PubMed]
    [Google Scholar]
  26. Imamura S, Asayama M. Sigma factors for cyanobacterial transcription. Gene Regul Syst Bio 2009; 3:65–87 [View Article] [PubMed]
    [Google Scholar]
  27. Flores C, Santos M, Pereira SB, Mota R, Rossi F et al. The alternative sigma factor SigF is a key player in the control of secretion mechanisms in Synechocystis sp. PCC 6803. Environ Microbiol 2019; 21:343–359 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001111
Loading
/content/journal/micro/10.1099/mic.0.001111
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error