Multiple Rounds of Artificial Selection Promote Microbe Secondary Domestication—The Case of Cachaça Yeasts

Abstract

The study of microbe domestication has witnessed major advances that contribute to a better understanding of the emergence of artificially selected phenotypes and set the foundations of their rational improvement for biotechnology. Several features make Saccharomyces cerevisiae an ideal model for such a study, notably the availability of a catalogue of signatures of artificial selection and the extensive knowledge available on its biological processes. Here, we investigate with population and comparative genomics a set of strains used for cachaça fermentation, a Brazilian beverage based on the fermentation of sugar cane juice. We ask if the selective pressures posed by this fermentation have given rise to a domesticated lineage distinct from the ones already known, like wine, beer, bread, and sake yeasts. Our results show that cachaça yeasts derive from wine yeasts that have undergone an additional round of domestication, which we define as secondary domestication. As a consequence, cachaça strains combine features of wine yeasts, such as the presence of genes relevant for wine fermentation and advantageous gene inactivations, with features of beer yeasts like resistance to the effects of inhibitory compounds present in molasses. For other markers like those related to sulfite resistance and biotin metabolism our analyses revealed distributions more complex than previously reported that support the secondary domestication hypothesis. We propose a multilayered microbe domestication model encompassing not only transitions from wild to primarily domesticated populations, as in the case of wine yeasts, but also secondary domestications like those of cachaça yeasts.

Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination

“…For example, if the "out-of-China" origin proposed for the ancestral range of wild S. cerevisiae is correct [20,64], our findings predict that that only the Ty1' subfamily should be found in ancestral woodland strains of S. cerevisiae from China. Answers to these and other questions should be facilitated by advances in the assembly of noisy long-read datasets [16], and development of computational techniques to resolve the presence of canonical Ty1 and Ty1' sequences from abundant short-read datasets for S. cerevisiae [20,49,60,61,63,[65][66][67][68][69][70][71][72].…”

Vitamin requirements and biosynthesis in Saccharomyces cerevisiae

“…For example, the reference strain S288C (Goffeau et al, ) lacks these two genes and is unable to grow on CDMY lacking biotin (Nijkamp et al, ). In contrast, sake strains of S. cerevisiae (Wu, Ito, & Shimoi, ), S. cerevisiae strains isolated from cachaça fermentations (Barbosa et al, ), and the laboratory strains A364a (Hall & Dietrich, ) and CEN.PK113‐7D (Bracher et al, ; Nijkamp et al, ) do carry these two genes and exhibit growth, albeit very slowly, on CDMY without biotin. BIO6 has been proposed to have evolved from a duplication and neofunctionalization of BIO3 , after BIO3 and BIO4 had been simultaneously acquired by horizontal gene transfer, with BIO1 similarly having evolved from duplication and neofunctionalization of the uncharacterized ORF YJR154W (Hall & Dietrich, ).…”

“…For example, the reference strain S288C (Goffeau et al, 1996) lacks these two genes and is unable to grow on CDMY lacking biotin (Nijkamp et al, 2012). In contrast, sake strains of S. cerevisiae (Wu, Ito, & Shimoi, 2005), S. cerevisiae strains isolated from cachaça fermentations (Barbosa et al, 2018), and the laboratory strains A364a (Hall & Dietrich, 2007) In view of its 55% amino-acid sequence similarity with Escherichia coli BioA, BIO6 probably encodes an adenosylmethionine-8-amino-7-oxononanoate transaminase (Wu et al, 2005). The initial formation of the pimeloyl thioester in S. cerevisiae remains unclear.…”

Bioprospecting for brewers: Exploiting natural diversity for naturally diverse beers

“…Wine yeast strains have been employed to brew beer and vice versa, whereas S. cerevisiae ale yeast has also been employed for lager brewing (Gallone et al, ). Wine yeast has also been discovered in cachaça fermentations, where evidence of secondary domestication is evident (Barbosa et al, ).…”