|
|
Time-scale separation and stochasticity conspire to impact phenotypic dynamics in the canonical and inverted Bacillus subtilis core genetic regulation circuits |
Lijie Hao1, Zhuoqin Yang1, Marc Turcotte2( ) |
1. School of Mathematics and Systems Science and LMIB, Beihang University, Beijing 100191, China 2. University of Texas at Dallas, Richardson, TX 75080, USA |
|
|
Abstract Background: In this work, we study two seemingly unrelated aspects of core genetic nonlinear dynamical control of the competence phenotype in Bacillus subtilis, a common Gram-positive bacterium living in the soil. Methods: We focus on hitherto unchartered aspects of the dynamics by exploring the effect of time-scale separation between transcription and translation and, as well, the effect of intrinsic molecular stochasticity. We consider these aspects of regulatory control as two possible evolutionary handles. Results: Hence, using theory and computations, we study how the onset of oscillations breaks the excitability-based competence phenotype in two topologically close evolutionary-competing circuits: the canonical “wild-type” regulation circuit selected by Evolution and the corresponding indirect-feedback inverted circuit that failed to be selected by Evolution, as was shown elsewhere, due to dynamical reasons. Conclusions: Relying on in-silico perturbation of the living state, we show that the canonical core genetic regulation of excitability-based competence is more robust against switching to phenotype-breaking oscillations than the inverted feedback organism. We show how this is due to time-scale separation and stochasticity.
|
Keywords
Bacillus subtilis
competence
gene regulation
deterministic dynamics
stochastic dynamics
|
Corresponding Author(s):
Marc Turcotte
|
Online First Date: 22 October 2018
Issue Date: 22 March 2019
|
|
1 |
A.Eldar, and M. B. Elowitz, (2010) Functional roles for noise in genetic circuits. Nature, 467, 167–173.
https://doi.org/10.1038/nature09326
pmid: 20829787
|
2 |
T.Cağatay, , M.Turcotte, , M. B.Elowitz, , J.Garcia-Ojalvo, and G. M.Süel, (2009) Architecture-dependent noise discriminates functionally analogous differentiation circuits. Cell, 139, 512–522
https://doi.org/10.1016/j.cell.2009.07.046.
pmid: 19853288
|
3 |
D.Schultz, E. Ben Jacob, J. N.Onuchic and P. G.Wolynes (2007) Molecular level stochastic model for competence cycles in Bacillus subtilis. Proc. Natl. Acad. Sci. USA., 104, 17582–17587.
https://doi.org/10.1073/pnas.0707965104
pmid: 17962411
|
4 |
M.Turcotte, J. Garcia-Ojalvo and G. M.Süel (2008) A genetic timer through noise-induced stabilization of an unstable state. Proc. Natl. Acad. Sci. USA, 105, 15732–15737..
https://doi.org/10.1073/pnas.0806349105
pmid: 18836072
|
5 |
G. M.Süel, J. Garcia-Ojalvo, L. M.Liberman and M. B.Elowitz (2006) An excitable gene regulatory circuit induces transient cellular differentiation. Nature, 440, 545–550..
https://doi.org/10.1038/nature04588
pmid: 16554821
|
6 |
G. M.Süel, R. P. Kulkarni, J.Dworkin, J.Garcia-Ojalvo and M. B.Elowitz (2007) Tunability and noise dependence in differentiation dynamics. Science, 315, 1716–1719..
https://doi.org/10.1126/science.1137455
pmid: 17379809
|
7 |
D.Dubnau (1999) DNA uptake in bacteria. Annu. Rev. Microbiol., 53, 217–244..
https://doi.org/10.1146/annurev.micro.53.1.217
pmid: 10547691
|
8 |
A. D.Grossman (1995) Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu. Rev. Genet., 29, 477–508..
https://doi.org/10.1146/annurev.ge.29.120195.002401
pmid: 8825484
|
9 |
D.Dubnau (1991) Genetic competence in Bacillus subtilis. Microbiol. Rev ., 55,395
|
10 |
D.Dubnau (1991) The regulation of genetic competence in Bacillus subtilis. Mol. Microbiol., 5, 11–18..
https://doi.org/10.1111/j.1365-2958.1991.tb01820.x
pmid: 1901615
|
11 |
W.Ma, A. Trusina, H.El-Samad, W. A.Lim and C.Tang (2009) Defining network topologies that can achieve biochemical adaptation. Cell, 138, 760–773..
https://doi.org/10.1016/j.cell.2009.06.013
pmid: 19703401
|
12 |
J.Zhang, Z. Yuan, H. X.Li and T.Zhou (2010) Architecture-dependent robustness and bistability in a class of genetic circuits. Biophys. J., 99, 1034–1042..
https://doi.org/10.1016/j.bpj.2010.05.036
pmid: 20712986
|
13 |
E. D.Levy (2010) A simple definition of structural regions in proteins and its use in analyzing interface evolution. J. Mol. Biol., 403, 660–670..
https://doi.org/10.1016/j.jmb.2010.09.028
pmid: 20868694
|
14 |
P. L.Kastritis and A. M.Bonvin (2013) Molecular origins of binding affinity: seeking the Archimedean point. Curr. Opin. Struct. Biol., 23, 868–877..
https://doi.org/10.1016/j.sbi.2013.07.001
pmid: 23876790
|
15 |
P. L.Kastritis, J. P. G. L. Rodrigues, G. E. Folkers, R.Boelens and A. M. J. J.Bonvin (2014) Proteins feel more than they see: fine-tuning of binding affinity by properties of the non-interacting surface. J. Mol. Biol., 426, 2632–2652..
https://doi.org/10.1016/j.jmb.2014.04.017
pmid: 24768922
|
16 |
A.Rosanova, A. Colliva, M.Osella and M.Caselle (2017) Modelling the evolution of transcription factor binding preferences in complex eukaryotes. Sci. Rep., 7, 7596.
https://doi.org/10.1038/s41598-017-07761-0
pmid: 28790414
|
17 |
J.Echave and C. O. Wilke (2017) Biophysical models of protein evolution: understanding the patterns of evolutionary sequence divergence. Annu. Rev. Biophys., 46, 85–103..
https://doi.org/10.1146/annurev-biophys-070816-033819
pmid: 28301766
|
18 |
D. T.Gillespie (1976) A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J. Comput. Phys., 22, 403–434..
https://doi.org/10.1016/0021-9991(76)90041-3
|
19 |
D. T.Gillespie (1977) Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem., 81, 2340–2361..
https://doi.org/10.1021/j100540a008
|
20 |
D. T.Gillespie (2001) Approximate accelerated stochastic simulation of chemically reacting systems. J. Chem. Phys., 115, 1716–1733..
https://doi.org/10.1063/1.1378322
|
21 |
D. T.Gillespie (1976) A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J. Comput. Phys., 22, 403–434..
https://doi.org/10.1016/0021-9991(76)90041-3
|
22 |
D. T.Gillespie (1977) Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem., 81, 2340–2361..
https://doi.org/10.1021/j100540a008
|
23 |
D. T.Gillespie (1991) Markov Processes: An Introduction for Physical Scientists. Manhattan: Academic Press
|
24 |
D. T.Gillespie (2007) Stochastic simulation of chemical kinetics. Annu. Rev. Phys. Chem., 58, 35–55..
https://doi.org/10.1146/annurev.physchem.58.032806.104637
pmid: 17037977
|
25 |
E. J. Doedel(1986) AUTO: software for continuation and bifurcation problems in ordinary differential equations. California Institute of Technology, 12, 791–802
|
26 |
B.Ermentrout (2011) XPP-Aut
|
27 |
E. D.Conrad (2011) Oscill8
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|