Tunable cell differentiation via reprogrammed mating-type switching.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
17 Sep 2024
17 Sep 2024
Historique:
received:
28
02
2024
accepted:
03
09
2024
medline:
18
9
2024
pubmed:
18
9
2024
entrez:
17
9
2024
Statut:
epublish
Résumé
This study introduces a synthetic biology approach that reprograms the yeast mating-type switching mechanism for tunable cell differentiation, facilitating synthetic microbial consortia formation and cooperativity. The underlying mechanism was engineered into a genetic logic gate capable of inducing asymmetric sexual differentiation within a haploid yeast population, resulting in a consortium characterized by mating-type heterogeneity and tunable population composition. The utility of this approach in microbial consortia cooperativity was demonstrated through the sequential conversion of xylan into xylose, employing haploids of opposite mating types each expressing a different enzyme of the xylanolytic pathway. This strategy provides a versatile framework for producing and fine-tuning functionally heterogeneous yet isogenic yeast consortia, furthering the advancement of microbial consortia cooperativity and offering additional avenues for biotechnological applications.
Identifiants
pubmed: 39289346
doi: 10.1038/s41467-024-52282-w
pii: 10.1038/s41467-024-52282-w
doi:
Substances chimiques
Xylose
A1TA934AKO
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8163Subventions
Organisme : National University of Singapore (NUS)
ID : NUHSRO/2020/077/MSC/02/SB
Organisme : National Research Foundation Singapore (National Research Foundation-Prime Minister's office, Republic of Singapore)
ID : NRF-MSG-2023-0003
Organisme : National Research Foundation Singapore (National Research Foundation-Prime Minister's office, Republic of Singapore)
ID : NRF-CRP27-2021-0004
Organisme : National Research Foundation Singapore (National Research Foundation-Prime Minister's office, Republic of Singapore)
ID : NRF-NRFI05-2019-0004
Organisme : Agency for Science, Technology and Research (A*STAR)
ID : I2301E0021
Informations de copyright
© 2024. The Author(s).
Références
McCarty, N. S. & Ledesma-Amaro, R. Synthetic biology tools to engineer microbial communities for biotechnology. Trends Biotechnol. 37, 181–197 (2019).
pubmed: 30497870
pmcid: 6340809
Momeni, B. Division of labor: how microbes split their responsibility. Curr. Biol. 28, R697–R699 (2018).
pubmed: 29920261
van Gestel, J., Vlamakis, H. & Kolter, R. Division of labor in biofilms: the ecology of cell differentiation. Microbiol. Spectr. 3, MB-0002-2014 (2015).
West, S. A. & Cooper, G. A. Division of labour in microorganisms: an evolutionary perspective. Nat. Rev. Microbiol. 14, 716–723 (2016).
pubmed: 27640757
Hacquard, S. et al. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17, 603–616 (2015).
pubmed: 25974302
Brenner, K., You, L. & Arnold, F. H. Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol. 26, 483–489 (2008).
pubmed: 18675483
Shong, J., Jimenez Diaz, M. R. & Collins, C. H. Towards synthetic microbial consortia for bioprocessing. Curr. Opin. Biotechnol. 23, 798–802 (2012).
pubmed: 22387100
Molinari, S. et al. A synthetic system for asymmetric cell division in Escherichia coli. Nat. Chem. Biol. 15, 917–924 (2019).
pubmed: 31406375
pmcid: 6702073
Mushnikov, N. V., Fomicheva, A., Gomelsky, M. & Bowman, G. R. Inducible asymmetric cell division and cell differentiation in a bacterium. Nat. Chem. Biol. 15, 925–931 (2019).
pubmed: 31406376
pmcid: 7439754
Haber, J. E. Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191, 33–64 (2012).
pubmed: 22555442
pmcid: 3338269
Hanson, S. J. & Wolfe, K. H. An evolutionary perspective on yeast mating-type switching. Genetics 206, 9–32 (2017).
Hicks, J., Strathern, J. N. & Klar, A. J. S. Transposable mating type genes in Saccharomyces cerevisiae. Nature 282, 478–483 (1979).
pubmed: 388235
Strathern, J., Hicks, J. & Herskowitz, I. Control of cell type in yeast by the mating type locus. The α1–α2 hypothesis. J. Mol. Biol. 147, 357–372 (1981).
pubmed: 7031257
Herschbach, B. M., Arnaud, M. B. & Johnson, A. D. Transcriptional repression directed by the yeast α2 protein in vitro. Nature 370, 309–311 (1994).
pubmed: 8035881
Herskowitz, I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52, 536–553 (1988).
pubmed: 3070323
pmcid: 373162
Haber, J. E. & George, J. P. A mutation that permits the expression of normally silent copies of mating-type information in Saccharomyces cerevisiae. Genetics 93, 13–35 (1979).
pubmed: 16118901
pmcid: 1217820
Takizawa, P. A., Sil, A., Swedlow, J. R., Herskowitz, I. & Vale, R. D. Actin-dependent localization of an RNA encoding a cell-fate determinant in the yeast. Nature 389, 90–93 (1997).
pubmed: 9288973
Long, R. M. et al. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277, 383–387 (1997).
pubmed: 9219698
Bobola, N., Jansen, R. P., Shin, T. H. & Nasmyth, K. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 84, 699–709 (1996).
pubmed: 8625408
Sil, A. & Herskowitz, I. Identification of an asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell 84, 711–722 (1996).
pubmed: 8625409
Cosma, M. P. Ordered recruitment: gene-specific mechanism of transcription activation. Mol. Cell 10, 227–236 (2002).
pubmed: 12191469
Stillman, D. J. Dancing the cell cycle two-step: regulation of yeast G1-cell-cycle genes by chromatin structure. Trends Biochem. Sci. 38, 467–475 (2013).
pubmed: 23870664
pmcid: 3771362
Ray, B. L., White, C. I. & Haber, J. E. Heteroduplex formation and mismatch repair of the ‘stuck’ mutation during mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 5372–5380 (1991).
pubmed: 1922052
pmcid: 361613
Haber, J. E., Savage, W. T., Raposa, S. M., Weiffenbach, B. & Rowe, L. B. Mutations preventing transpositions of yeast mating type alleles. Proc. Natl Acad. Sci. USA 77, 2824–2828 (1980).
pubmed: 6248869
pmcid: 349497
Merlini, L., Dudin, O. & Martin, S. G. Mate and fuse: how yeast cells do it. Open Biol. 3, 130008 (2013).
pubmed: 23466674
pmcid: 3718343
Mackay, V. & Manney, T. R. Mutations affecting sexual conjugation and related processes in Saccharomyces cerevisiae. II. Genetic analysis of nonmating mutants. Genetics 76, 273–288 (1974).
pubmed: 4595644
pmcid: 1213065
Jenness, D. D., Burkholder, A. C. & Hartwell, L. H. Binding of α-factor pheromone to yeast a cells: chemical and genetic evidence for an α-factor receptor. Cell 35, 521–529 (1983).
pubmed: 6360378
Kurjan, J. Alpha-factor structural gene mutations in Saccharomyces cerevisiae: effects on alpha-factor production and mating. Mol. Cell Biol. 5, 787–796 (1985).
pubmed: 3887136
pmcid: 366783
Hagen, D. C., McCaffrey, G. & Sprague, G. F. Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc. Natl Acad. Sci. USA 83, 1418–1422 (1986).
pubmed: 3006051
pmcid: 323087
Michaelis, S. & Herskowitz, I. The a-factor pheromone of Saccharomyces cerevisiae is essential for mating. Mol. Cell Biol. 8, 1309–1318 (1988).
pubmed: 3285180
pmcid: 363277
Dohrmann, P. R. et al. Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase. Genes Dev. 6, 93–104 (1992).
pubmed: 1730413
Koch, C., Moll, T., Neuberg, M., Ahorn, H. & Nasmyth, K. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261, 1551–1557 (1993).
pubmed: 8372350
Measday, V., McBride, H., Moffat, J., Stillman, D. & Andrews, B. Interactions between Pho85 cyclin-dependent kinase complexes and the Swi5 transcription factor in budding yeast. Mol. Microbiol 35, 825–834 (2000).
pubmed: 10692159
Jansen, R. P., Dowzer, C., Michaelis, C., Galova, M. & Nasmyth, K. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin Myo4p and other cytoplasmic proteins. Cell 84, 687–697 (1996).
pubmed: 8625407
Niessing, D., Jansen, R. P., Pohlmann, T. & Feldbrügge, M. mRNA transport in fungal top models. Wiley Interdiscip. Rev. RNA 9, e1453 (2018).
Niednery, A., Edelmanny, F. T. & Niessing, D. Of social molecules: the interactive assembly of ASH1 mRNA-transport complexes in yeast. RNA Biol. 11, 998–1009 (2014).
Heng, Y. C. & Foo, J. L. Development of destabilized mCherry fluorescent proteins for applications in the model yeast Saccharomyces cerevisiae. Biotechnol. Notes 3, 108–112 (2022).
Pothoulakis, G. & Ellis, T. Construction of hybrid regulated mother-specific yeast promoters for inducible differential gene expression. PLoS ONE 13, e0194588 (2018).
pubmed: 29566038
pmcid: 5864024
Nasmyth, K. At least 1400 base pairs of 5′-flanking DNA is required for the correct expression of the HO gene in yeast. Cell 42, 213–223 (1985).
pubmed: 3893741
Harrison, M. C., LaBella, A. L., Hittinger, C. T. & Rokas, A. The evolution of the GALactose utilization pathway in budding yeasts. Trends Genet. 38, 97–106 (2022).
pubmed: 34538504
Martínez, A. A., Conboy, A., Buskirk, S. W., Marad, D. A. & Lang, G. I. Long-term adaptation to galactose as a sole carbon source selects for mutations outside the canonical GAL oathway. J. Mol. Evol. 91, 46–59 (2023).
pubmed: 36482210
Törrönen, A. et al. The two major xylanases from Trichoderma reesei: characterization of both enzymes and genes. Bio/Technology 10, 1461–1465 (1992).
pubmed: 1369024
Guirimand, G. et al. Cell-surface display technology and metabolic engineering of: Saccharomyces cerevisiae for enhancing xylitol production from woody biomass. Green Chem. 21, 1795–1808 (2019).
Katahira, S., Fujita, Y., Mizuike, A., Fukuda, H. & Kondo, A. Construction of a xylan-fermenting yeast strain through codisplay of xylanolytic enzymes on the surface of xylose-utilizing Saccharomyces cerevisiae cells. Appl. Environ. Microbiol. 70, 5407–5414 (2004).
pubmed: 15345427
pmcid: 520881
Apel, A. R., Ouellet, M., Szmidt-Middleton, H., Keasling, J. D. & Mukhopadhyay, A. Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae. Sci. Rep. 6, 1–10 (2016).
Inokuma, K. et al. Enhanced cell-surface display and secretory production of cellulolytic enzymes with Saccharomyces cerevisiae Sed1 signal peptide. Biotechnol. Bioeng. 113, 2358–2366 (2016).
pubmed: 27183011
Van Der Vaart, J. M. et al. Comparison of cell wall proteins of Saccharomyces cerevisiae as anchors for cell surface expression of heterologous proteins. Appl. Environ. Microbiol. 63, 615–620 (1997).
pubmed: 9023939
pmcid: 168351
Yang, X. et al. Development of novel surface display platforms for anchoring heterologous proteins in Saccharomyces cerevisiae. Microb. Cell Fact. 18, 1–10 (2019).
Grayhack, E. J. The yeast alpha 1 and MCM1 proteins bind a single strand of their duplex DNA recognition site. Mol. Cell. Biol. 12, 3573–3582 (1992).
pubmed: 1630462
pmcid: 364623
Flessel, M. C., Brake, A. J. & Thorner, J. The MF alpha 1 gene of Saccharomyces cerevisiae: genetic mapping and mutational analysis of promoter elements. Genetics 121, 223–236 (1989).
pubmed: 2659433
pmcid: 1203612
Hagen, D. C., Bruhn, L., Westby, C. A. & Sprague, G. F. Transcription of alpha-specific genes in Saccharomyces cerevisiae: DNA sequence requirements for activity of the coregulator alpha 1. Mol. Cell. Biol. 13, 6866–6875 (1993).
pubmed: 8413280
pmcid: 364749
Jarvis, E. E., Hagen, D. C. & Sprague, G. F. Identification of a DNA segment that is necessary and sufficient for alpha-specific gene control in Saccharomyces cerevisiae: implications for regulation of alpha-specific and a-specific genes. Mol. Cell. Biol. 8, 309–320 (1988).
pubmed: 3275872
pmcid: 363126
Peng, H. et al. A molecular toolkit of cross-feeding strains for engineering synthetic yeast communities. Nat. Microbiol. 9, 848–863 (2024).
pubmed: 38326570
pmcid: 10914607
Brachmann, C. B. et al. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115–132 (1998).
pubmed: 9483801
Ekino, K., Kwon, I., Goto, M., Yoshino, S. & Furukawa, K. Functional analysis of HO gene in delayed homothallism in Saccharomyces cerevisiae wy2. Yeast 15, 451–458 (1999).
pubmed: 10234783
Meiron, H., Nahon, E. & Raveh, D. Identification of the heterothallic mutation in HO-endonuclease of S. cerevisiae using HO/ho chimeric genes. Curr. Genet 28, 367–373 (1995).
pubmed: 8590483
Gietz, R. D. & Schiestl, R. H. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2, 31–34 (2007).
pubmed: 17401334