Coevolution with bacteria drives the evolution of aerobic fermentation in Lachancea kluyveri

Abstract

The Crabtree positive yeasts, such as Saccharomyces cerevisiae, prefer fermentation to respiration, even under fully aerobic conditions. The selective pressures that drove the evolution of this trait remain controversial because of the low ATP yield of fermentation compared to respiration. Here we propagate experimental populations of the weak-Crabtree yeast Lachancea kluyveri, in competitive co-culture with bacteria. We find that L. kluyveri adapts by producing quantities of ethanol lethal to bacteria and evolves several of the defining characteristics of Crabtree positive yeasts. We use precise quantitative analysis to show that the rate advantage of fermentation over aerobic respiration is insufficient to provide an overall growth advantage. Thus, the rapid consumption of glucose and the utilization of ethanol are essential for the success of the aerobic fermentation strategy. These results corroborate that selection derived from competition with bacteria could have provided the impetus for the evolution of the Crabtree positive trait.

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.…”

“…Both co-cultures and control cultures were passaged as shown in Fig 2A . For co-culture evolution, one species of bacteria was introduced at a time (for example, shown as red, yellow or green) in the order previously reported [ 16 , 20 ] and shown in Fig 2B . After co-incubation for 44 hours, streptomycin (100 μg/mL) was added to kill “off” bacteria.…”

“…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 ].…”

Microbial and Chemical Diversity of Traditional Non-Cereal Based Alcoholic Beverages of Sub-Saharan Africa

“…This suggests that Saccharomyces yeasts are the most dominant alcoholic fermentation microorganisms [75][76][77]. Even in the presence of oxygen, S. cerevisiae, is the predominant yeast species responsible for the production of ethanol [78,79]. The production of ethanol, toxic to other microbes, has been hypothesized to be a niche defense mechanism for S. cerevisiae [42].…”

“…Like any other alcoholic beverages, the conversion of the sugary substrate leads to increased nutritional components. The aromatic complexity of the wine is due to the production of compounds produced such as esters, carbonyls, alcohols, phenols, acids, sulphur compounds, terpenes, hydrocarbons, nitrogen compounds, and lactone [63,79,80,126].…”