Nitric oxide increases biofilm formation in Saccharomyces cerevisiae by activating the transcriptional factor Mac1p and thereby regulating the transmembrane protein Ctr1

Abstract

Background Biofilms with immobilized cells encased in extracellular polymeric substance are beneficial for industrial fermentation. Their formation is regulated by various factors, including nitric oxide (NO), which is recognized as a quorum-sensing and signal molecule. The mechanisms by which NO regulates bacterial biofilms have been studied extensively and deeply, but were rarely studied in fungi. In this study, we observed the effects of low concentrations of NO on biofilm formation in Saccharomyces cerevisiae. Transcriptional and proteomic analyses were applied to study the mechanism of this regulation. Results Adding low concentrations of NO donors (SNP and NOC-18) enhanced biofilm formation of S. cerevisiae in immobilized carriers and plastics. Transcriptional and proteomic analyses revealed that expression levels of genes regulated by the transcription factor Mac1p was upregulated in biofilm cells under NO treatment. MAC1 promoted yeast biofilm formation which was independent of flocculation gene FLO11 . Increased copper and iron contents, both of which were controlled by Mac1p in the NO-treated and MAC1 -overexpressing cells, were not responsible for the increased biofilm formation. CTR1 , one out of six genes regulated by MAC1 , plays an important role in biofilm formation. Moreover, MAC1 and CTR1 contributed to the cells’ resistance to ethanol by enhanced biofilm formation. Conclusions These findings suggest that a mechanism for NO-mediated biofilm formation, which involves the regulation of CTR1 expression levels by activating its transcription factor Mac1p, leads to enhanced biofilm formation. The role of CTR1 protein in yeast biofilm formation may be due to the hydrophobic residues in its N-terminal extracellular domain, and further research is needed. This work offers a possible explanation for yeast biofilm formation regulated by NO and provides approaches controlling biofilm formation in industrial immobilized fermentation by manipulating expression of genes involved in biofilm formation. Electronic supplementary material The online version of this article (10.1186/s13068-019-1359-1) contains supplementary material, which is available to authorized users.

HGT in the human and skin commensal Malassezia : A bacterially derived flavohemoglobin is required for NO resistance and host interaction

“…Conversely, we propose that Malassezia flavohemoglobins are important for the commensal lifestyle of Malassezia through regulation of NO homeostasis, a hypothesis corroborated by down-regulation of genesencoding putative virulence factors (i.e., allergens and lipases) in our transcriptomic analyses. Another hypothesis is that the HGTmediated acquisition of flavohemoglobins might be important to mediate Malassezia response to NO that is produced by sympatric microbial communities and acts as a quorum signaling molecule, as reported in bacteria (48) and in S. cerevisiae (49).…”

Spatially structured yeast communities: Understanding structure formation and regulation with omics tools

“…The formation of these biofilms is also potentiated by NO, where transcriptomics together with proteomics revealed the importance of Ctr1p (plasma membrane copper transporter) and its transcriptional regulator Mac1p. This regulation was independent of Flo11p and concentrations of Cu and Fe ions [65] .…”

Cell Cycle Progression Influences Biofilm Formation in Saccharomyces cerevisiae 1308

“…FLO1 and FLO5 confer cell-cell viscosity and contribute to flocculation ( 30 ). FLO11 encodes a flocculating protein that enhances cell-matrix adhesion and could play a role in development of biofilm in liquid medium ( 31 , 32 ). The results of the qRT-PCR analysis revealed that the expression levels of FLO1 and FLO5 were upregulated in Δ sic1 and Δ cln3 , while the expression of FLO11 was upregulated by 1-fold in Δ sic1 but downregulated by 2-fold in Δ cln3.…”

“…Plate-wash assay was to test the ability of invasive growth of different strains. The ability of invasive growth depends on cell-substrate adhesion, which plays a vital role in biofilm formation ( 31 ). In this study, Δ sic1 and Δ cln3 formed more colonies on YPD plates than did WT.…”