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Molecular mechanism of flocculation self-recognition in yeast and its role in mating and survival

Katty VY Goossens, Francesco S Ielasi, Intawat Nookaew, Ingeborg Stals UGent, Livan Alonso-Sarduy, Luk Daenen, Sebastiaan E Van Mulders, Catherine Stassen, Rudy GE van Eijsden,, Verena Siewers, et al. (2015) MBIO. 6(2).
abstract
We studied the flocculation mechanism at the molecular level by determining the atomic structures of N-Flo1p and N-Lg-Flo1p in complex with their ligands. We show that they have similar ligand binding mechanisms but distinct carbohydrate specificities and affinities, which are determined by the compactness of the binding site. We characterized the glycans of Flo1p and their role in this binding process and demonstrate that glycan-glycan interactions significantly contribute to the cell-cell adhesion mechanism. Therefore, the extended flocculation mechanism is based on the self-interaction of Flo proteins and this interaction is established in two stages, involving both glycan-glycan and protein-glycan interactions. The crucial role of calcium in both types of interaction was demonstrated: Ca-2(+) takes part in the binding of the carbohydrate to the protein, and the glycans aggregate only in the presence of Ca-2(+). These results unify the generally accepted lectin hypothesis with the historically first-proposed "Ca-2(+)-bridge" hypothesis. Additionally, a new role of cell flocculation is demonstrated; i.e., flocculation is linked to cell conjugation and mating, and survival chances consequently increase significantly by spore formation and by introduction of genetic variability. The role of Flo1p in mating was demonstrated by showing that mating efficiency is increased when cells flocculate and by differential transcriptome analysis of flocculating versus nonflocculating cells in a low-shear environment (microgravity). The results show that a multicellular clump (floc) provides a uniquely organized multicellular ultrastructure that provides a suitable microenvironment to induce and perform cell conjugation and mating. IMPORTANCE Yeast cells can form multicellular clumps under adverse growth conditions that protect cells from harsh environmental stresses. The floc formation is based on the self-interaction of Flo proteins via an N-terminal PA14 lectin domain. We have focused on the flocculation mechanism and its role. We found that carbohydrate specificity and affinity are determined by the accessibility of the binding site of the Flo proteins where the external loops in the ligand-binding domains are involved in glycan recognition specificity. We demonstrated that, in addition to the Flo lectin-glycan interaction, glycan-glycan interactions also contribute significantly to cell-cell recognition and interaction. Additionally, we show that flocculation provides a uniquely organized multicellular ultrastructure that is suitable to induce and accomplish cell mating. Therefore, flocculation is an important mechanism to enhance long-term yeast survival.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
FILAMENTOUS GROWTH, HAPLOID INVASIVE GROWTH, GENE-EXPRESSION, PSEUDOHYPHAL DIFFERENTIATION, SIGNALING PATHWAYS, SACCHAROMYCES-CEREVISIAE, N-TERMINAL DOMAIN, CARBOHYDRATE-CARBOHYDRATE INTERACTIONS, SNF1 PROTEIN-KINASE, TRANSCRIPTIONAL ACTIVATOR
journal title
MBIO
MBIO
editor
Yup Lee Sang
volume
6
issue
2
article number
UNSP e00427
pages
16 pages
Web of Science type
Article
Web of Science id
000355312400033
JCR category
MICROBIOLOGY
JCR impact factor
6.975 (2015)
JCR rank
13/123 (2015)
JCR quartile
1 (2015)
ISSN
2150-7511
DOI
10.1128/mBio.00427-15
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
6885035
handle
http://hdl.handle.net/1854/LU-6885035
date created
2015-07-27 09:46:51
date last changed
2017-03-09 12:51:14
@article{6885035,
  abstract     = {We studied the flocculation mechanism at the molecular level by determining the atomic structures of N-Flo1p and N-Lg-Flo1p in complex with their ligands. We show that they have similar ligand binding mechanisms but distinct carbohydrate specificities and affinities, which are determined by the compactness of the binding site. We characterized the glycans of Flo1p and their role in this binding process and demonstrate that glycan-glycan interactions significantly contribute to the cell-cell adhesion mechanism. Therefore, the extended flocculation mechanism is based on the self-interaction of Flo proteins and this interaction is established in two stages, involving both glycan-glycan and protein-glycan interactions. The crucial role of calcium in both types of interaction was demonstrated: Ca-2(+) takes part in the binding of the carbohydrate to the protein, and the glycans aggregate only in the presence of Ca-2(+). These results unify the generally accepted lectin hypothesis with the historically first-proposed {\textacutedbl}Ca-2(+)-bridge{\textacutedbl} hypothesis. Additionally, a new role of cell flocculation is demonstrated; i.e., flocculation is linked to cell conjugation and mating, and survival chances consequently increase significantly by spore formation and by introduction of genetic variability. The role of Flo1p in mating was demonstrated by showing that mating efficiency is increased when cells flocculate and by differential transcriptome analysis of flocculating versus nonflocculating cells in a low-shear environment (microgravity). The results show that a multicellular clump (floc) provides a uniquely organized multicellular ultrastructure that provides a suitable microenvironment to induce and perform cell conjugation and mating.
IMPORTANCE Yeast cells can form multicellular clumps under adverse growth conditions that protect cells from harsh environmental stresses. The floc formation is based on the self-interaction of Flo proteins via an N-terminal PA14 lectin domain. We have focused on the flocculation mechanism and its role. We found that carbohydrate specificity and affinity are determined by the accessibility of the binding site of the Flo proteins where the external loops in the ligand-binding domains are involved in glycan recognition specificity. We demonstrated that, in addition to the Flo lectin-glycan interaction, glycan-glycan interactions also contribute significantly to cell-cell recognition and interaction. Additionally, we show that flocculation provides a uniquely organized multicellular ultrastructure that is suitable to induce and accomplish cell mating. Therefore, flocculation is an important mechanism to enhance long-term yeast survival.},
  articleno    = {UNSP e00427},
  author       = {Goossens, Katty VY and Ielasi, Francesco S and Nookaew, Intawat and Stals, Ingeborg and Alonso-Sarduy, Livan and Daenen, Luk and Van Mulders, Sebastiaan E and Stassen, Catherine and van Eijsden,, Rudy GE and Siewers, Verena and Delvaux, Freddy R and Kasas, Sandor and Nielsen, Jens and Devreese, Bart and Willaert, Ronnie G},
  editor       = {Sang, Yup Lee},
  issn         = {2150-7511},
  journal      = {MBIO},
  keyword      = {FILAMENTOUS GROWTH,HAPLOID INVASIVE GROWTH,GENE-EXPRESSION,PSEUDOHYPHAL DIFFERENTIATION,SIGNALING PATHWAYS,SACCHAROMYCES-CEREVISIAE,N-TERMINAL DOMAIN,CARBOHYDRATE-CARBOHYDRATE INTERACTIONS,SNF1 PROTEIN-KINASE,TRANSCRIPTIONAL ACTIVATOR},
  language     = {eng},
  number       = {2},
  pages        = {16},
  title        = {Molecular mechanism of flocculation self-recognition in yeast and its role in mating and survival},
  url          = {http://dx.doi.org/10.1128/mBio.00427-15},
  volume       = {6},
  year         = {2015},
}

Chicago
Goossens, Katty VY, Francesco S Ielasi, Intawat Nookaew, Ingeborg Stals, Livan Alonso-Sarduy, Luk Daenen, Sebastiaan E Van Mulders, et al. 2015. “Molecular Mechanism of Flocculation Self-recognition in Yeast and Its Role in Mating and Survival.” Ed. Yup Lee Sang. Mbio 6 (2).
APA
Goossens, K. V., Ielasi, F. S., Nookaew, I., Stals, I., Alonso-Sarduy, L., Daenen, L., Van Mulders, S. E., et al. (2015). Molecular mechanism of flocculation self-recognition in yeast and its role in mating and survival. (Y. L. Sang, Ed.)MBIO, 6(2).
Vancouver
1.
Goossens KV, Ielasi FS, Nookaew I, Stals I, Alonso-Sarduy L, Daenen L, et al. Molecular mechanism of flocculation self-recognition in yeast and its role in mating and survival. Sang YL, editor. MBIO. 2015;6(2).
MLA
Goossens, Katty VY, Francesco S Ielasi, Intawat Nookaew, et al. “Molecular Mechanism of Flocculation Self-recognition in Yeast and Its Role in Mating and Survival.” Ed. Yup Lee Sang. MBIO 6.2 (2015): n. pag. Print.