Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese
Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese
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DOI：
10.1128/mbio.02445-19
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发表时间：
2019-09-01
期刊：
影响因子：
6.4
通讯作者：
Wolfe, Benjamin E.
中科院分区：
文献类型：
--
作者：
Bodinaku, Ina;Shaffer, Jason;Wolfe, Benjamin E.
发酵食品为微生物的自然种群提供了新的生态机会，通过资源丰富的底物的连续发酵来进化。比较基因组数据已经重建了适应食品环境的微生物的进化历史，但对于大多数发酵食品微生物来说，缺乏直接证明驯化过程的实验研究。在这里，我们表明，在适应奶酪，野生青霉霉菌的表型和代谢组学性状迅速变化，产生驯化的表型与用于制造卡门贝尔和其他开花的奶酪的工业文化的属性相似。在短短几周的时间里，在奶酪上连续传代的野生青霉菌株的种群减少了色素、孢子和真菌毒素的产生。驯化的菌株在挥发性代谢物的产生方面也有显著的变化，从产生泥土味或发霉的挥发性化合物（例如，土臭素）到脂肪和干酪挥发物（例如，2-壬酮、2-十一烷酮）。RNA测序表明驯化菌株中356个基因的表达显著降低，这些下调基因中富含许多次级代谢产物产生途径。通过操纵存在的邻近微生物物种和整体资源的可用性，我们证明了有限的竞争和高营养的奶酪环境促进快速性状演变的青霉molds.Importance丝状真菌的工业文化被用来添加独特的美学和风味的奶酪和其他微生物食品。这些微生物如何适应生活在食品环境中通常是未知的，因为大多数微生物驯化是无意的。我们的工作表明，野生霉菌密切相关的发酵剂培养青霉菌卡门贝蒂可以很容易地失去性状，并迅速转向生产所需的香气化合物。除了通过实验证明P. camemberti的假定驯化途径外，我们的工作表明野生青霉菌分离株可以快速驯化，以在发酵食品中产生新的风味和美学。
Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates. Comparative genomic data have reconstructed the evolutionary histories of microbes adapted to food environments, but experimental studies directly demonstrating the process of domestication are lacking for most fermented food microbes. Here, we show that during adaptation to cheese, phenotypic and metabolomic traits of wild Penicillium molds rapidly change to produce domesticated phenotypes with properties similar to those of the industrial cultures used to make Camembert and other bloomy rind cheeses. Over a period of just a few weeks, populations of wild Penicillium strains serially passaged on cheese had reduced pigment, spore, and mycotoxin production. Domesticated strains also had a striking change in volatile metabolite production, shifting from production of earthy or musty volatile compounds (e.g., geosmin) to fatty and cheesy volatiles (e.g., 2-nonanone, 2-undecanone). RNA sequencing demonstrated a significant decrease in expression of 356 genes in domesticated strains, with an enrichment of many secondary metabolite production pathways in these downregulated genes. By manipulating the presence of neighboring microbial species and overall resource availability, we demonstrate that the limited competition and high nutrient availability of the cheese environment promote rapid trait evolution of Penicillium molds.IMPORTANCE Industrial cultures of filamentous fungi are used to add unique aesthetics and flavors to cheeses and other microbial foods. How these microbes adapted to live in food environments is generally unknown as most microbial domestication is unintentional. Our work demonstrates that wild molds closely related to the starter culture Penicillium camemberti can readily lose traits and quickly shift toward producing desirable aroma compounds. In addition to experimentally demonstrating a putative domestication pathway for P. camemberti, our work suggests that wild Penicillium isolates could be rapidly domesticated to produce new flavors and aesthetics in fermented foods.