Robust stochastic Turing patterns in the development of a one-dimensional cyanobacterial organism

PLoS Biol. 2018 May 4;16(5):e2004877. doi: 10.1371/journal.pbio.2004877. eCollection 2018 May.

Abstract

Under nitrogen deprivation, the one-dimensional cyanobacterial organism Anabaena sp. PCC 7120 develops patterns of single, nitrogen-fixing cells separated by nearly regular intervals of photosynthetic vegetative cells. We study a minimal, stochastic model of developmental patterns in Anabaena that includes a nondiffusing activator, two diffusing inhibitor morphogens, demographic fluctuations in the number of morphogen molecules, and filament growth. By tracking developing filaments, we provide experimental evidence for different spatiotemporal roles of the two inhibitors during pattern maintenance and for small molecular copy numbers, justifying a stochastic approach. In the deterministic limit, the model yields Turing patterns within a region of parameter space that shrinks markedly as the inhibitor diffusivities become equal. Transient, noise-driven, stochastic Turing patterns are produced outside this region, which can then be fixed by downstream genetic commitment pathways, dramatically enhancing the robustness of pattern formation, also in the biologically relevant situation in which the inhibitors' diffusivities may be comparable.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anabaena / genetics
  • Anabaena / growth & development*
  • Anabaena / metabolism
  • Bacterial Proteins / metabolism
  • Models, Biological*
  • Oxidoreductases / metabolism
  • Stochastic Processes

Substances

  • Bacterial Proteins
  • PatS protein, Anabaena
  • HetR protein, Bacteria
  • Oxidoreductases
  • HetN protein, Anabaena

Grants and funding

Siegried and Irma Ullman Professorial Chair to J.S. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. COSMOS ITN EU to D.F. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Italian Ministero dell'Istruzione dell'Universita e della Ricerca (MIUR) http://www.miur.gov.it/ to D.F. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Minerva Stiftung http://www.minerva.mpg.de/ to J.S. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.