The Evolutionary Imprint of Domestication on Genome Variation and Function of the Filamentous Fungus Aspergillus oryzae

Abstract

Summary The domestication of animals, plants and microbes fundamentally transformed the lifestyle and demography of the human species [1]. Although the genetic and functional underpinnings of animal and plant domestication are well understood, little is known about microbe domestication [2–6]. We systematically examined genome-wide sequence and functional variation between the domesticated fungus Aspergillus oryzae, whose saccharification abilities humans have harnessed for thousands of years to produce sake, soy sauce and miso from starch-rich grains, and its wild relative A. flavus, a potentially toxigenic plant and animal pathogen [7]. We discovered dramatic changes in the sequence variation and abundance profiles of genes and wholesale primary and secondary metabolic pathways between domesticated and wild relative isolates during growth on rice. Through selection by humans, our data suggest that an atoxigenic lineage of A. flavus gradually evolved into a “cell factory” for enzymes and metabolites involved in the saccharification process. These results suggest that whereas animal and plant domestication was largely driven by Neolithic “genetic tinkering” of developmental pathways, microbe domestication was driven by extensive remodeling of metabolism.

MALDI-TOF Mass Spectrometry: Any Use for Aspergilli?

“…In our study, MALDI-TOF MS was shown to easily differentiate A. flavus and A. oryzae on the species level, and interestingly, clinical isolates of A. oryzae and A. flavus formed separate clusters with their corresponding reference strains, and both the clusters could be distinguished from those of A. parasiticus and A. alliaceus, respectively [35]. Although A. flavus produces harmful aflatoxins while A. oryzae does not, nonaflatoxigenic isolates of A. flavus are highly related to A. oryzae, and this is consistent with the hypothesis that an atoxigenic lineage of A. flavus has gradually evolved into a domesticated A. oryzae through selection by humans [36]. As several non(afla)toxigenic A. flavus isolates are phenotypically more similar to A. oryzae than to other A. flavus isolates, a molecular-phenotypic approach such as MALDI-TOF MS could be very useful for discriminating toxigenic from atoxigenic strains within the A. flavus species [24].…”

Deletion of creB in Aspergillus oryzae Increases Secreted Hydrolytic Enzyme Activity

“…We have shown that A. oryzae DAR3699 has a mutation in the promoter of its creB gene; that it has many phenotypes consistent with loss of creB function, including strong growth on acet- amide, weak growth on proline, quinate, or arabinose, resistance to molybdate, high protease secretion, and little or no inhibition of spore germination by glucose; and that deleting creB in this strain does not change the phenotype. A. oryzae arose through the ancient domestication of Aspergillus flavus and has undergone genetic changes during its centuries of use in Asian food and beverage production (29). Our data suggest that for A. oryzae DAR3699, one of these genetic changes is likely to have been partial or complete loss of creB function.…”

Transcriptional Changes in the Transition from Vegetative Cells to Asexual Development in the Model Fungus Aspergillus nidulans

“…Thus, this powerful technique arises as an efficient tool for transcriptomic analyses in the genus Aspergillus, as shown in 2010 by Wang and coworkers (11), who published the first RNA-seq-based transcriptomic study of this genus. In these last 2 years, the RNA-seq-based studies involving Aspergillus species analyzed the temperature effect on secondary metabolite synthesis, biofilm formation, the response to lignocellulose, or domestication in A. fumigatus, A. flavus, A. niger, or A. oryzae, respectively (11)(12)(13)(14)(15).…”