Abstract
Microbial species occupying the same ecological niche or codeveloping during a fermentation process can exchange metabolites and mutualistically influence each other’s metabolic states. For instance, yeast can excrete amino acids, thereby cross-feeding lactic acid bacteria unable to grow without an external amino acid supply. The yeast membrane transporters involved in amino acid excretion remain poorly known. Using a yeast mutant overproducing and excreting threonine (Thr) and its precursor homoserine (Hom), we show that excretion of both amino acids involves the Aqr1, Qdr2, and Qdr3 proteins of the Drug H+-Antiporter Family (DHA1) family. We further investigated Aqr1 as a representative of these closely related amino acid exporters. In particular, structural modeling and molecular docking coupled to mutagenesis experiments and excretion assays enabled us to identify residues in the Aqr1 substrate-binding pocket that are crucial for Thr and/or Hom export. We then co-cultivated yeast and Lactobacillus fermentum in an amino-acid-free medium and found a yeast mutant lacking Aqr1, Qdr2, and Qdr3 to display a reduced ability to sustain the growth of this lactic acid bacterium, a phenotype not observed with strains lacking only one of these transporters. This study highlights the importance of yeast DHA1 transporters in amino acid excretion and mutualistic interaction with lactic acid bacteria.
Highlights
Amino acids are among the most abundant nitrogenous compounds in all cells
A more recent study has demonstrated that metabolically active yeast cells growing on a nitrogen-rich medium excrete metabolites, especially amino acids, and that this excretion enables cocultivated lactic acid bacteria to proliferate (Ponomarova et al, 2017)
In this study we have investigated further the role of DHA1family transporters in amino acid excretion and their potential contribution to cross-feeding lactic acid bacteria
Summary
Amino acids are among the most abundant nitrogenous compounds in all cells They serve a wide range of purposes, as building blocks for protein synthesis, as nitrogen or carbon sources, as metabolic intermediates, and as chemical messengers (Gutiérrez-Preciado et al, 2010). Rose showed that yeast cells, when faced with a suboptimal nutrient supply, excrete several compounds They notably excrete amino acids in sufficient quantity to meet the amino acid requirements of co-cultivated lactic acid bacteria (Challinor and Rose, 1954). In the same study it was shown that yeast cells lacking arginine permease activity excrete arginine, as shown by their ability to cross-feed an arginine auxotroph This indicated that amino acid importers can potentially mediate retention of specific amino acids that naturally leak out of the cell (Grenson, 1973). It is established that microorganisms occupying the same ecological niche or codeveloping during food product fermentation can exchange metabolites, notably amino acids, and mutualistically influence each other’s metabolic differentiation (Martin-Rendon et al, 1993; Scherlach et al, 2013; D’Souza et al, 2018; Tshikantwa et al, 2018)
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