Microbial Succession and Flavor Production in the Fermented Dairy Beverage Kefir.
Kefir is a putatively health-promoting dairy beverage that is produced when a kefir grain, consisting of a consortium of microorganisms, is added to milk to initiate a natural fermentation. Here, a detailed analysis was carried out to determine how the microbial population, gene content, and flavor of three kefirs from distinct geographic locations change over the course of 24-h fermentations. Metagenomic sequencing revealed thatLactobacillus kefiranofacienswas the dominant bacterial species in kefir during early stages of fermentations but thatLeuconostoc mesenteroidesbecame more prevalent in later stages. This pattern is consistent with an observation that genes involved in aromatic amino acid biosynthesis were absent fromL. kefiranofaciensbut were present inL. mesenteroides. Additionally, these shifts in the microbial community structure, and associated pathways, corresponded to changes in the levels of volatile compounds. Specifically,Acetobacterspp. correlated with acetic acid;Lactobacillusspp. correlated with carboxylic acids, esters and ketones;Leuconostocspp. correlated with acetic acid and 2,3-butanedione; andSaccharomycesspp. correlated with esters. The correlation data suggest a causal relationship between microbial taxa and flavor that is supported by observations that addition ofL. kefiranofaciensNCFB 2797 increased the levels of esters and ketones whereas addition ofL. mesenteroides213M0 increased the levels of acetic acid and 2,3-butanedione. Finally, we detected genes associated with probiotic functionalities in the kefir microbiome. Our results illustrate the dynamic nature of kefir fermentations and microbial succession patterns therein and can be applied to optimize the fermentation processes, flavors, and health-related attributes of this and other fermented foods.IMPORTANCETraditional fermented foods represent relatively low-complexity microbial environments that can be used as model microbial communities to understand how microbes interact in natural environments. Our results illustrate the dynamic nature of kefir fermentations and microbial succession patterns therein. In the process, the link between individual species, and associated pathways, with flavor compounds is revealed and several genes that could be responsible for the purported gut health-associated benefits of consuming kefir are identified. Ultimately, in addition to providing an important fundamental insight into microbial interactions, this information can be applied to optimize the fermentation processes, flavors, and health-related attributes of this and other fermented foods.
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Institute, University College Cork, Co. Cork, Ireland; Microbiology Department, University College Cork, Co. Cork, Ireland.
Aaron M
AM
Walsh
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Institute, University College Cork, Co. Cork, Ireland.
Fiona
F
Crispie
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland.
Kieran
K
Kilcawley
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Institute, University College Cork, Co. Cork, Ireland.
Orla
O
O'Sullivan
School of Food and Nutritional Sciences, University College Cork, Co. Cork, Ireland.
Maurice G
MG
O'Sullivan
APC Microbiome Institute, University College Cork, Co. Cork, Ireland; Microbiology Department, University College Cork, Co. Cork, Ireland.
Marcus J
MJ
Claesson
Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland; APC Microbiome Institute, University College Cork, Co. Cork, Ireland.
Paul D
PD
Cotter
dairy; flavor; kefir; metagenomics; microbiota