Diverse microbial communities in kefir, a traditional grainy fermented milk-based drink, achieve stable coexistence through intricate orchestration of metabolite dynamics in space and time, reports a new study.

The authors use metabolomics, transcriptomics, and large-scale mapping of inter-species interactions to show microorganisms poorly suited for milk emerge as the dominant species through metabolic cooperation and the uneven distribution of microbial communities between the milk and grain components in kefir.

These findings from the European Molecular Biology Laboratory (EMBL) and Cambridge University’s Patil group and collaborators, are published in the article “Polarization of microbial communities between competitive and cooperative metabolism” published in Nature Microbiology.

Microbial communities can alter in composition and yet maintain stable coexistence of diverse species. The mechanisms underlying this long-term dynamic coexistence remain unclear largely because of limited system-wide studies focusing on engineered communities or synthetic microbial assemblies. Understanding the underlying mechanism of microbial community dynamics can help develop therapeutic strategies for several diseases that have been linked to compositional changes in the microbiomes of the gut and other physiological habitats.

“The kefir grain acts as a base camp for the kefir community, from which community members colonize the milk in a complex yet organized and cooperative manner,” says Kiran Patil, PhD, group leader and corresponding author. “We see this phenomenon in kefir, and then we see it’s not limited to kefir. If you look at the whole world of microbiomes, cooperation is also a key to their structure and function.”

The authors show, during fermentation of milk, kefir grains—a polysaccharide matrix synthesized by kefir microorganisms—grow in mass but remain unchanged in composition. The milk, on the other hand, is sequentially colonized such that early microbial members provide metabolites like amino acids and lactate, to make it possible for subsequent microbial communities to survive and thrive in the milk.

“Cooperation allows them to do something they couldn’t do alone,” says Patil. “It is particularly fascinating how L. kefiranofaciens, which dominates the kefir community, uses kefir grains to bind together all other microbes that it needs to survive—much like the ruling ring of the Lord of the Rings. One grain to bind them all.”

Considered by many to be a ‘superfood,’ Kefir is of North Caucasian origin that later became popular in Russia, Eastern Europe and Israel. Kefir is composed of grains that look like lightly mashed cauliflower in fermented milk containing bacteria and yeast. Its many purported health benefits include improved digestion and reduction of blood pressure and blood glucose levels.

Kefir grains
Kefir grains—a polysaccharide matrix synthesized by kefir microorganisms [A. Kniesel]

Kefir is made using kefir grains that can’t be artificially made but must come from another batch of kefir. The grains are added to milk to ferment and grow. Between one and four days, the kefir grains consume the nutrients available to them, grow in size and number, and the kefir process is complete. The grains are then removed and added to fresh milk to start a new kefir cycle.

“People were storing milk in sheepskins and noticed these grains that emerged kept their milk from spoiling, so they could store it longer,” says Sonja Blasche, PhD, a postdoc in the Patil group and joint first author of the paper. “Because milk spoils fairly easily, finding a way to store it longer was of huge value.”

Kefir provides an easy-to-culture model microbial community for scientific studies on metabolic interactions. Although similar to yogurt in being a fermented and cultured dairy product rich in probiotics, kefir’s microbial community is far larger than yogurt’s and includes yeast, in addition to bacteria. With around 40 microbial species, kefir offers a natural “Goldilocks zone of complexity” says Patil, improving over earlier studies that have focused on only two or three interacting species and yet not too unwieldy to study in detail.

The team collected 15 Kefir samples from around Germany and other places and profiled the compositional diversity in microbial communities in the samples collected from the various geographical locations.

“Our first step was to look at how the samples grow. Kefir microbial communities have many member species with individual growth patterns that adapt to their current environment. This means fast- and slow-growing species and some that alter their speed according to nutrient availability,” Blasche says. “This is not unique to the kefir community. However, the kefir community had a lot of lead time for co-evolution to bring it to perfection, as they have stuck together for a long time already.”

Related studies from the group have shown that competitive communities retain diverse metabolic capacities to exploit all available nutrients whereas cooperative communities include species that have lost key metabolic genes so that they must depend on each other for survival (auxotrophic species). The authors note, while both competitive and cooperative communities are prevalent, the cooperators seem to be more successful in terms of higher abundance and occupying diverse habitats.

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