Yeast–bacteria competition induced new metabolic traits through large-scale genomic rearrangements in Lachancea kluyveri

Abstract

Large-scale chromosomal rearrangements are an important source of evolutionary novelty that may have reshaped the genomes of existing yeast species. They dramatically alter genome organization and gene expression fueling a phenotypic leap in response to environmental constraints. Although the emergence of such signatures of genetic diversity is thought to be associated with human exploitation of yeasts, less is known about the driving forces operating in natural habitats. Here we hypothesize that an ecological battlefield characteristic of every autumn when fruits ripen accounts for the genomic innovations in natural populations. We described a long-term cross-kingdom competition experiment between Lachancea kluyveri and five species of bacteria. Now, we report how we further subjected the same yeast to a sixth species of bacteria, Pseudomonas fluorescens, resulting in the appearance of a fixed and stably inherited large-scale genomic rearrangement in two out of three parallel evolution lines. The 'extra-banded' karyotype, characterized by a higher fitness and an elevated fermentative capacity, conferred the emergence of new metabolic traits in most carbon sources and osmolytes. We tracked down the event to a duplication and translocation event involving a 261-kb segment. Such an experimental setup described here is an attractive method for developing industrial strains without genetic engineering strategies.

Genome dynamics and evolution in yeasts: A long-term yeast-bacteria competition experiment

“…We set up a laboratory evolution experiment mimicking the natural environment characteristic of cross-kingdom competition for sugars in nature when fruits ripen leading to availability of excess sugars for a short period of time as previously reported [ 16 , 20 , 39 ]. In more detail, a total of 18 yeasts from the family Saccharomycetaceae covering a wide phylogenetic background spanning over 250 million years of evolutionary history [ 36 ] were cultured in the presence as well as in the absence of bacteria.…”

“…cerevisiae [ 11 , 14 ]. Other distant relatives of the baker´s yeasts have also been reported to respond to environmental perturbations by genome restructuring [ 15 , 16 ].…”

“…Bacteria are potential “hurdles” that could influence the evolution of adaptive life strategies in yeast by rewiring of their genetic networks; for example, carbon metabolism pathways and regulatory networks [ 16 , 20 ]. They secrete antifungal compounds such as chitinases [ 21 , 22 ], central carbon metabolism-impairing compounds such as weak organic acids, prions and long-chain fatty acids [ 23 – 29 ].…”

Reconstruction and analysis of genome-scale metabolic model of weak Crabtree positive yeast Lachancea kluyveri

“…From the previously generated experimental data [18,41,42], the accuracy of the prediction of the model was evaluated. Using the similar substrate and oxygen uptake rate as measured in the experiment, the specific growth rate and the product secretion rates were evaluated in silico by FBA.…”

An assessment of serial co-cultivation approach for generating novel Zymomonas mobilis strains

“…The evolved strains conferred altered chemical complexity in produced wine [9]. Zhou et al showed that long term bacterial-yeast competition induced chromosomal arrangements in the yeast, rendering stress-tolerance, altered metabolism and other physiological features in the yeast Lachancea kluyveri [10]. In addition to promoting mutation, co-culture has also been shown to promote the production of particular metabolites in Streptomyces species, which were otherwise not expressed in pure monoculture [11,12].…”