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L-histidine inhibits biofilm formation and FLO11-associated phenotypes in Saccharomyces cerevisiae flor yeasts.

Bou Zeidan M, Zara G, Viti C, Decorosi F, Mannazzu I, Budroni M, Giovannetti L, Zara S - PLoS ONE (2014)

Bottom Line: L-histidine completely inhibited growth and its effect on viability was inversely related to Flo11p expression.Accordingly, L-histidine did not affect the viability of the Δflo11 and S288c strains.Also, L-histidine dramatically decreased air-liquid biofilm formation and adhesion to polystyrene of the flor yeasts with no effect on the transcription level of the Flo11p gene.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Agraria, University of Sassari, Sassari, Italy.

ABSTRACT
Flor yeasts of Saccharomyces cerevisiae have an innate diversity of Flo11p which codes for a highly hydrophobic and anionic cell-wall glycoprotein with a fundamental role in biofilm formation. In this study, 380 nitrogen compounds were administered to three S. cerevisiae flor strains handling Flo11p alleles with different expression levels. S. cerevisiae strain S288c was used as the reference strain as it cannot produce Flo11p. The flor strains generally metabolized amino acids and dipeptides as the sole nitrogen source, although with some exceptions regarding L-histidine and histidine containing dipeptides. L-histidine completely inhibited growth and its effect on viability was inversely related to Flo11p expression. Accordingly, L-histidine did not affect the viability of the Δflo11 and S288c strains. Also, L-histidine dramatically decreased air-liquid biofilm formation and adhesion to polystyrene of the flor yeasts with no effect on the transcription level of the Flo11p gene. Moreover, L-histidine modified the chitin and glycans content on the cell-wall of flor yeasts. These findings reveal a novel biological activity of L-histidine in controlling the multicellular behavior of yeasts [corrected].

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High throughput and cluster analysis of nitrogen metabolism of different S. cerevisiae strains.The nitrogen uptake of the A9, M23, V80 and S288c strains was measured using the phenotype microarray technique. (A) Cluster analysis (Pearson coefficient, UPGMA) for similarity regrouping of tested strains on all nitrogen sources. IN was used as a parameter. Values at the nodes represent cophenic correlation coefficients. (B) Each square represents the growth of one strain in the PM wells supplied with the indicated L-histidine containing dipeptide, as a nitrogen source. The extent of growth was generated from the tetrazolium dye reduction during 96 h and represented by the intensity of coloration; white squares mean no growth and dark black squares mean abundant growth. Dipeptides are grouped respect to the N-terminus amino acid.
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pone-0112141-g001: High throughput and cluster analysis of nitrogen metabolism of different S. cerevisiae strains.The nitrogen uptake of the A9, M23, V80 and S288c strains was measured using the phenotype microarray technique. (A) Cluster analysis (Pearson coefficient, UPGMA) for similarity regrouping of tested strains on all nitrogen sources. IN was used as a parameter. Values at the nodes represent cophenic correlation coefficients. (B) Each square represents the growth of one strain in the PM wells supplied with the indicated L-histidine containing dipeptide, as a nitrogen source. The extent of growth was generated from the tetrazolium dye reduction during 96 h and represented by the intensity of coloration; white squares mean no growth and dark black squares mean abundant growth. Dipeptides are grouped respect to the N-terminus amino acid.

Mentions: According to the PM technique, the electron flow that results from the catabolism of nutritional substrates induces a shift in the tetrazolium dye to a purple color. When catabolism occurs at a subnormal rate, this results in a decrease in the electron flow and decreased intensity of the purple color [31]. On this basis, PM plates were used to test the ability of the strains to catabolize 380 different nitrogen sources, photographed every 15 min, to generate a growth curve for each well that primarily reflected dye reduction [25]. After 96 h of static incubation, PM analysis showed that the four strains differed greatly in the use of the nitrogen sources. In particular, while A9 and M23 catabolized 128 and 121 nitrogen sources, respectively, this number dramatically decreased for V80 and S288c, which used just 14 and 40 nitrogen sources, respectively (Fig. S1). Differences were observed also for the catabolism rate of nitrogen sources among strains. On the basis of cluster analysis of PM results, the four strains were ascribed to two groups, one consisting of A9 and M23, and the other one containing V80 and S288c (Fig. 1A). A9 and M23, but not V80 and S288c, grew slightly on different nucleotides, such as cytosine and adenine. They metabolized single L-amino acids, such as L-arginine, L-glutamine, L-phenylalanine, L-serine and L-tryptophan and showed high metabolic rates when fed with dipeptides containing alanine, valine, serine and threonine on their N-terminus. In parallel, all of the strains showed clear inability to metabolize dipeptides containing proline, asparagine, cysteine and lysine at their N-terminus. Notably, none of the strains grew in the L-histidine wells (Fig. S1). At the same time, A9 and M23 clearly did not grow in the presence of dipeptides containing L-histidine at their C- and/or N-terminus. On the contrary, strains V80 and S288c showed high and specific metabolic rates toward these dipeptides (Fig. 1B).


L-histidine inhibits biofilm formation and FLO11-associated phenotypes in Saccharomyces cerevisiae flor yeasts.

Bou Zeidan M, Zara G, Viti C, Decorosi F, Mannazzu I, Budroni M, Giovannetti L, Zara S - PLoS ONE (2014)

High throughput and cluster analysis of nitrogen metabolism of different S. cerevisiae strains.The nitrogen uptake of the A9, M23, V80 and S288c strains was measured using the phenotype microarray technique. (A) Cluster analysis (Pearson coefficient, UPGMA) for similarity regrouping of tested strains on all nitrogen sources. IN was used as a parameter. Values at the nodes represent cophenic correlation coefficients. (B) Each square represents the growth of one strain in the PM wells supplied with the indicated L-histidine containing dipeptide, as a nitrogen source. The extent of growth was generated from the tetrazolium dye reduction during 96 h and represented by the intensity of coloration; white squares mean no growth and dark black squares mean abundant growth. Dipeptides are grouped respect to the N-terminus amino acid.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4219837&req=5

pone-0112141-g001: High throughput and cluster analysis of nitrogen metabolism of different S. cerevisiae strains.The nitrogen uptake of the A9, M23, V80 and S288c strains was measured using the phenotype microarray technique. (A) Cluster analysis (Pearson coefficient, UPGMA) for similarity regrouping of tested strains on all nitrogen sources. IN was used as a parameter. Values at the nodes represent cophenic correlation coefficients. (B) Each square represents the growth of one strain in the PM wells supplied with the indicated L-histidine containing dipeptide, as a nitrogen source. The extent of growth was generated from the tetrazolium dye reduction during 96 h and represented by the intensity of coloration; white squares mean no growth and dark black squares mean abundant growth. Dipeptides are grouped respect to the N-terminus amino acid.
Mentions: According to the PM technique, the electron flow that results from the catabolism of nutritional substrates induces a shift in the tetrazolium dye to a purple color. When catabolism occurs at a subnormal rate, this results in a decrease in the electron flow and decreased intensity of the purple color [31]. On this basis, PM plates were used to test the ability of the strains to catabolize 380 different nitrogen sources, photographed every 15 min, to generate a growth curve for each well that primarily reflected dye reduction [25]. After 96 h of static incubation, PM analysis showed that the four strains differed greatly in the use of the nitrogen sources. In particular, while A9 and M23 catabolized 128 and 121 nitrogen sources, respectively, this number dramatically decreased for V80 and S288c, which used just 14 and 40 nitrogen sources, respectively (Fig. S1). Differences were observed also for the catabolism rate of nitrogen sources among strains. On the basis of cluster analysis of PM results, the four strains were ascribed to two groups, one consisting of A9 and M23, and the other one containing V80 and S288c (Fig. 1A). A9 and M23, but not V80 and S288c, grew slightly on different nucleotides, such as cytosine and adenine. They metabolized single L-amino acids, such as L-arginine, L-glutamine, L-phenylalanine, L-serine and L-tryptophan and showed high metabolic rates when fed with dipeptides containing alanine, valine, serine and threonine on their N-terminus. In parallel, all of the strains showed clear inability to metabolize dipeptides containing proline, asparagine, cysteine and lysine at their N-terminus. Notably, none of the strains grew in the L-histidine wells (Fig. S1). At the same time, A9 and M23 clearly did not grow in the presence of dipeptides containing L-histidine at their C- and/or N-terminus. On the contrary, strains V80 and S288c showed high and specific metabolic rates toward these dipeptides (Fig. 1B).

Bottom Line: L-histidine completely inhibited growth and its effect on viability was inversely related to Flo11p expression.Accordingly, L-histidine did not affect the viability of the Δflo11 and S288c strains.Also, L-histidine dramatically decreased air-liquid biofilm formation and adhesion to polystyrene of the flor yeasts with no effect on the transcription level of the Flo11p gene.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Agraria, University of Sassari, Sassari, Italy.

ABSTRACT
Flor yeasts of Saccharomyces cerevisiae have an innate diversity of Flo11p which codes for a highly hydrophobic and anionic cell-wall glycoprotein with a fundamental role in biofilm formation. In this study, 380 nitrogen compounds were administered to three S. cerevisiae flor strains handling Flo11p alleles with different expression levels. S. cerevisiae strain S288c was used as the reference strain as it cannot produce Flo11p. The flor strains generally metabolized amino acids and dipeptides as the sole nitrogen source, although with some exceptions regarding L-histidine and histidine containing dipeptides. L-histidine completely inhibited growth and its effect on viability was inversely related to Flo11p expression. Accordingly, L-histidine did not affect the viability of the Δflo11 and S288c strains. Also, L-histidine dramatically decreased air-liquid biofilm formation and adhesion to polystyrene of the flor yeasts with no effect on the transcription level of the Flo11p gene. Moreover, L-histidine modified the chitin and glycans content on the cell-wall of flor yeasts. These findings reveal a novel biological activity of L-histidine in controlling the multicellular behavior of yeasts [corrected].

Show MeSH
Related in: MedlinePlus