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Volume 169, Issue 11

Identification of a morphogene required for tapered filament termini in filamentous cyanobacteria Open Access

Abstract

Although the photosynthetic cyanobacteria are monophyletic, they exhibit substantial morphological diversity across species, and even within an individual species due to phenotypic plasticity in response to life cycles and environmental signals. This is particularly prominent among the multicellular filamentous cyanobacteria. One example of this is the appearance of tapering at the filament termini. However, the morphogenes controlling this phenotype and the adaptive function of this morphology are not well defined. Here, using the model filamentous cyanobacterium ATCC29133 (PCC73102), we identify , a morphogene required for the development of tapered filament termini. The gene is specifically expressed in developing hormogonia, motile trichomes where the tapered filament morphology is observed, and encodes a protein containing putative amidase_3 and glucosaminidase domains, implying a function in peptidoglycan hydrolysis. Deletion of abolished filament tapering inidcating that TftA plays a role in remodelling the cell wall to produce tapered filaments. Genomic conservation of specifically in filamentous cyanobacteria indicates this is likely to be a conserved mechanism among these organisms. Finally, motility assays indicate that filaments with tapered termini migrate more efficiently through dense substratum, providing a plausible biological role for this morphology.

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  • Accepted:
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Keyword(s): cell morphology, phenotypic plasticity , cyanobacteria , morphogene and motility
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-11-16
2024-05-19
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References

  1. Stanier RY, Deruelles J, Rippka R, Herdman M, Waterbury JB. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 1979; 111:1–61 [View Article]
     [Google Scholar]
  2. Springstein BL, Nürnberg DJ, Weiss GL, Pilhofer M, Stucken K. Structural determinants and their role in cyanobacterial morphogenesis. Life 2020; 10:10 [View Article] [PubMed]
     [Google Scholar]
  3. Montgomery BL. Mechanisms and fitness implications of photomorphogenesis during chromatic acclimation in cyanobacteria. J Exp Bot 2016; 67:4079–4090 [View Article] [PubMed]
     [Google Scholar]
  4. Terauchi K, Montgomery BL, Grossman AR, Lagarias JC, Kehoe DM. RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol Microbiol 2004; 51:567–577 [View Article] [PubMed]
     [Google Scholar]
  5. Bordowitz JR, Montgomery BL. Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon. J Bacteriol 2008; 190:4069–4074 [View Article] [PubMed]
     [Google Scholar]
  6. Singh SP, Montgomery BL. Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in Fremyella diplosiphon. Mol Microbiol 2014; 93:167–182 [View Article] [PubMed]
     [Google Scholar]
  7. Risser DD. Hormogonium development and motility in filamentous cyanobacteria. Appl Environ Microbiol 2023; 89:e0039223 [View Article] [PubMed]
     [Google Scholar]
  8. Zuniga EG, Figueroa NM, Gonzalez A, Pantoja AP, Risser DD. The hybrid histidine kinase HrmK is an early-acting factor in the hormogonium gene regulatory network. J Bacteriol 2020; 202:e00675-19 [View Article] [PubMed]
     [Google Scholar]
  9. 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]
  10. 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]
  11. 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 2016; 198:137–147 [View Article] [PubMed]
     [Google Scholar]
  12. Cai YP, Wolk CP. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 1990; 172:3138–3145 [View Article] [PubMed]
     [Google Scholar]
  13. Harwood TV, Risser DD. The primary transcriptome of hormogonia from a filamentous cyanobacterium defined by cappable-seq. Microbiology 2021; 167: [View Article] [PubMed]
     [Google Scholar]
  14. Wei TF, Ramasubramanian TS, Golden JW. Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 1994; 176:4473–4482 [View Article] [PubMed]
     [Google Scholar]
  15. 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]
  16. Khayatan B, Bains DK, Cheng MH, Cho YW, Huynh J et al. A putative O-linked β-N-acetylglucosamine transferase is essential for hormogonium development and motility in the filamentous cyanobacterium Nostoc punctiforme. J Bacteriol 2017; 199:00075–17 [View Article] [PubMed]
     [Google Scholar]
  17. Lehner J, Berendt S, Dörsam B, Pérez R, Forchhammer K et al. Prokaryotic multicellularity: a nanopore array for bacterial cell communication. FASEB J 2013; 27:2293–2300 [View Article] [PubMed]
     [Google Scholar]
  18. Cho YW, Gonzales A, Harwood TV, Huynh J, Hwang Y et al. Dynamic localization of HmpF regulates type IV pilus activity and directional motility in the filamentous cyanobacterium Nostoc punctiforme. Mol Microbiol 2017; 106:252–265 [View Article] [PubMed]
     [Google Scholar]
  19. 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]
  20. Kuroda A, Sugimoto Y, Funahashi T, Sekiguchi J. Genetic structure, isolation and characterization of a Bacillus licheniformis cell wall hydrolase. Mol Gen Genet 1992; 234:129–137 [View Article] [PubMed]
     [Google Scholar]
  21. Nambu T, Minamino T, Macnab RM, Kutsukake K. Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J Bacteriol 1999; 181:1555–1561 [View Article] [PubMed]
     [Google Scholar]
  22. Hirano T, Minamino T, Macnab RM. The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase. J Mol Biol 2001; 312:359–369 [View Article] [PubMed]
     [Google Scholar]
  23. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021; 596:583–589 [View Article] [PubMed]
     [Google Scholar]
  24. Korndörfer IP, Danzer J, Schmelcher M, Zimmer M, Skerra A et al. The crystal structure of the bacteriophage PSA endolysin reveals a unique fold responsible for specific recognition of Listeria cell walls. J Mol Biol 2006; 364:678–689 [View Article] [PubMed]
     [Google Scholar]
  25. Hashimoto W, Ochiai A, Momma K, Itoh T, Mikami B et al. Crystal structure of the glycosidase family 73 peptidoglycan hydrolase FlgJ. Biochem Biophys Res Commun 2009; 381:16–21 [View Article] [PubMed]
     [Google Scholar]
  26. Caccamo PD, Brun YV. The molecular basis of noncanonical bacterial morphology. Trends Microbiol 2018; 26:191–208 [View Article] [PubMed]
     [Google Scholar]
  27. 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]
  28. 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]
  29. Stal LJ. Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol 1995; 131:1–32 [View Article] [PubMed]
     [Google Scholar]
  30. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci U S A 2013; 110:1053–1058 [View Article] [PubMed]
     [Google Scholar]
  31. Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc Natl Acad Sci U S A 2013; 110:1791–1796 [View Article] [PubMed]
     [Google Scholar]
  32. Guex N, Peitsch MC, Schwede T. Automated comparative protein structure modeling with SWISS-MODEL and SWISS-PdbViewer: a historical perspective. Electrophoresis 2009; 30 Suppl 1:S162–73 [View Article] [PubMed]
     [Google Scholar]
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Identification of a morphogene required for tapered filament termini in filamentous cyanobacteria
Microbiology 169, 001416 (2023); https://doi.org/10.1099/mic.0.001416
/content/journal/micro/10.1099/mic.0.001416
/content/journal/micro/10.1099/mic.0.001416
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