On pickles: biological and sociocultural links between fermented foods and the human gut microbiome

An ethnobiological approach to fermentation and the microbiome opens a dialogue between microbiology and social science. Much of this conversation has centered around microorganisms’ role in human metabolic function, the political implications of seeing microbes as enemies, neutral parties, or allies, and the ways in which human existence is made plural through microbial entanglement [17]. Given this contemporary moment of microbiomania [18] across the social and natural sciences, scholars are increasingly asking how socioecological practices including growing, preparing, and consuming fermented foods, sustain microbial communities, heritage foodways, and human health.

A range of biomedical research has shown how human gut microbiomes shift in response to environmental context. Such studies have found significant differences between small-scale rural and industrialized urban populations in Papua New Guinea [19], Russia [20], Burkina Faso [21], Tanzania, [5, 22], and in the Venezuelan Amazon and rural Malawai [23]. In addition to these comparative studies, other research suggests that the same human population can alter its gut microbiome composition by moving. Migrants who come from rural areas in Asia to the USA experienced a loss in microbiome diversity [24], while Hadza gut flora can shift seasonally as a function of foods available and consumed [22].

Such studies evaluate microorganisms with respect to their ability to alter gut ecology in ways that correct non-biodiverse or otherwise unhealthy bodies. Noting how this governance over “right” and “wrong” bodies is reminiscent of Foucauldian biopolitics, Paxson [25‐27] identifies a “microbiopolitics” inscribed in food safety regulations and everyday governance over human-microbe relationships in personal hygiene. Louis Pasteur’s germ theory and the fear that unhealthy citizens might spread disease through dangerous microbes inspired a range of state hygiene regulations, the biopolitical culmination of a world in which microbes are inherently dangerous and destabilizing to human wellbeing [27, 28]. As fermentation involves the intentional introduction of microbes, Paxson and others [18, 29] argue that fermenters occupy a post-Pasteurian ontological position in which some microbes may be dangerous, but others are helpful or neutral. Such microbial entanglements provide new ways for people to reframe microbial discourse away from the inherently perilous threats to bodies imagined by Pasteur and toward a world of promising interconnection [30, 31].

In reimagining relationships between people and microbes, Paxson contends that we can also reimagine relationships between people and institutions. Haraway [32] and Tsing [33] similarly leverage the post-Pastuerian logic of fermentation and composting to imagine communal transformation in the face of socioeconomic collapse. Following a collapse and genocide in ex-Yugoslavia, Jasarevic [34] argues that Bosnian kombucha starters help citizens begin to repair ethnonational distrust through microbial gifts and creative reorganizations of bacteria and yeast. Promising interconnection can lead to commercialization in the artisanal wine and kombucha industries, where scholars ask how producers, consumers, and regulators imagine microbiology in the context of food safety, consumer desire, and state oversight. In practice, these industries demand a microbiological citizenship in which stakeholders respect microbial beings as intentional agents that require extra-legal negotiations between producers and consumers [29, 35]. Where these scholars emphasize the present and future, some biological anthropologists also use microbes to imagine the past. Noting that pasteurization would not have been present in the paleoenvironmental context of Homo sapiens evolution, Speth [36] argues that the regulatory push to exclude microbes from contemporary industrial food systems, including the consumption of fermented foods, now contributes to dietary mismatches that negatively influence contemporary health outcomes. Other microbiome-curious paleoanthropologists investigate the opposite direction, analyzing the microbiota in preserved dental films to reconstruct past diets and ecologies [37, 38].

Land, states, soil, and microbes all meet in fermentation, where local socioecological variations in recipe and autochthonous bacteria transform vegetables and dairy products into distinctive foods. Much foodways scholarship demonstrates how foods are used to stake ethnic and other identity claims [39‐41]. Fermented foods are not subtle. The microbially rich worlds of fermented foods allow communities to stake identity claims that are both phenomenological, through the pungent sensations of fermented foods, and microbiological: Korean food scientists evoke microbes to argue that Kimchi is uniquely Korean and not Japanese [42]; far-right Hindu nationalists make claims to native microbiota from native cows in Indian soils to envision a pure, native agricultural state [43]; indigenous Siberian communities reclaim fermented meats to distinguish themselves from Russian assimilation [44]; communities hail Bulgarian yogurt [45, 46] or Ghanaian dawa-dawa [47] because they claim that these provide unique health benefits through unique Lactobacillus bacteria in the face of globalizing food systems. Beyond staking ethnic or community claims, fermentation builds new and imagined communities because ferments are live cultures and can be shared through active starter cultures and brines. Like Maussian gifts, they carry the spirit of the giver alongside particular tastes and sociopolitical meanings when shared [34, 48]. To share and consume these foods is to embrace wider relationships.

This perspective from food studies suggests that microbes in fermented foods and in bodies intersect with sociocultural notions of identity. Biologically, diet in general [49] and fermented food products in particular have been shown to influence the composition of human microbiomes [50], a point seized by Danone Yogurt’s nutritional research team [51]. However, determining the exact links between particular food products, including fermented foods is difficult outside of clinical settings. Fermented foods vary widely in the microbes they might introduce to the human microbiome because these foods are eaten as part of larger food systems and because a number of confounding sociocultural factors determining how people eat complicate how people ultimately encounter microbes. While private companies or local advocacy groups might promote the nutraceutical benefits of fermented foods [12, 52], ethnobiologists recognize as well that these foods rely on in-situ conservation of microbial and agricultural biodiversity [7, 8, 10], and folk microbiology to continue practicing and adapting this social food system.

Ethnobiologists interested in how fermented foods become part of larger food systems have looked to fermentation in the contexts of food sovereignty and food security. Ethnobotanists ask how fermentation secures access to taste and nutrition in the Balkans [7, 53] and across Europe generally [11, 12], while others track how wild plants introduce autochthonous bacteria that makes fermented beverages in the archaeological record [54, 55] and in the present [56, 57]. Fermentation is also emerging as a means for traditional knowledge revival, as when communities frustrated with the offerings of global agrifood networks turn to fermented food traditions to seek out distinctive tastes [25, 58, 59] or rediscover heritage recipes [60]. Through recipe-sharing networks, gift exchanges of microbial cultures [34], or workshops like the one profiled below, fermentation revivalists are working to conserve and cultivate local and heritage biodiversity down to the microbial level. Where private companies and regulatory systems grapple with a new politics of food safety [25, 29, 61], ethnobiologists are increasingly recognizing ways in which agrobiodiversity, traditional knowledge, and microbial diversity might go hand in hand [62].

This scholarship suggests two key questions that emerge from an attempt to combine cultural anthropology and microbiology in the study of ethnozymology. First, do the local and heritage recipes that give fermented foods their distinctive flavors result in measurable differences in the resulting food products? That is, is one sauerkraut microbiologically distinct from another in ways that have impacts on the human microbiome? Teams including the Benjamin Wolfe lab [63, 64] have been asking similar questions by inoculating gnotobiotic (microbe-free) cabbages to observe the results, while Marcellino et al. [65] examined differences in bacterial genera from French cheeses of differing regions. Although the resulting ecosystems appear to be similar with respect to microbial composition, cheese and sauerkraut microbes vary as a function of carbon assimilation and salt tolerance. This suggests that minor differences in craft process have profound impacts in what fermented food lovers perceive as taste. In an agricultural riff on microbial research, terroir, the sociocultural value of local environmental conditions in food, is here reimagined as a quantifiable local microbial ecology. Where ethnobiologists [8] and anthropologists [26] emphasize how microbes accumulate monetary value when artisanal practices are recognized as a microbial terroir, microbiologists [61, 65, 66] are tracking how aggregated culinary and landscape management decisions, ranging from wine barrels to cheese caves, affect microbial ecology in measurable and reproducible ways. These studies suggest that social and microbial cultures can be linked in productive ways.

Second, do microbial communities present in fermented foods influence the human microbiome in ways that have longstanding or beneficial effects? This is the argument made by researchers affiliated with the probiotics industry, such as the Danone Yogurt research team. This same kind of claim must also be regulated under a microbiopolitics that lends state support to microbial health. However, few studies track these interactions outside of clinical settings, in the spaces where people live and eat. Overwhelmingly, health and diet scholarship on fermentation and the microbiome is dominated by clinical or genetic approaches. One recent report with wide-ranging sociocultural implications on the influence of migration and dietary change on human microbiomes in the USA even employs community-based participatory research methods to collect its data, but relies entirely on quantitative and biomedical analysis to explain the relationship between migration, microbiome, food, and health [24]. While emphasizing the importance of subtle distinctions in place, conceptions of health, and dietary practices, these studies do not incorporate sociocultural qualitative data into their analysis. This is a missed opportunity because this research assumes but does not investigate the importance of local knowledge vested in communities that shape dynamic ecosystems and create possibilities for future socioecological relationships.

These are, fundamentally, sociocultural questions that have to do with how people live and eat. They represent the structuring conditions under which the microbial landscape of a fermented food and a human gut microbiome interact. To begin answering both questions, we conducted interviews, participant observation, and recipe and process elicitation in combination with the collection of biological samples of fermented foods and human stools at a 2018 workshop led by fermentation revivalist Sandor Katz [48, 67]. Katz runs a biannual 4-day fermentation workshop for experienced food fermenters at his homestead in Liberty, Tennessee. As the event asked participants to pay according to a sliding scale, we recognize that this particular group and workshop is not necessarily representative of all fermentation revivalists, let alone the broad and diverse population who regularly consumes fermented foods around the world. However, their experiences and diverse histories with fermentation and larger bodies of heritage foodways comprise a wide set of interesting perspectives. Given the hyper-local nature of microbiome research, even this small group can help to illuminate our larger research questions into the synergies between life experiences, place, and microbiome.

As social scientists who study biological and cultural diversity, we wanted to learn about the traditions that sustain microbial communities through fermentation. This led to a research design including both qualitative ethnographic elements as well as quantitative microbiological elements. Along with ten other fermentation enthusiasts, including school teachers, business owners, food professionals, and students, we learned to make microbially rich foods including kimchi, sake, tempeh, and yogurt. Drawing on the opportunities of event ethnography [68], in which a small team participates in and collects a variety of data from a larger event, we drew on the accessibility of this workshop and the eagerness of event participants to share information, speak with each other, discuss nuances in shared ideas, and develop new ways of approaching group and individual decisions. Andrew Flachs, a cultural anthropologist, held interviews with all consenting participants, recorded parts of the workshop, convened group discussions on cooking, fermenting, and heritage foods, asked participants to list recipes and outline social networks related to fermented foods, and kept field notes detailing participation and observation in the workshop. Joseph Orkin, an anthropologically trained geneticist, collected biological samples of the fermented foods at the workshop, including yogurt, pickled vegetables, kimchi, sauerkraut, and miso. To collect gut microbial data that we could then associate with the lived experiences of the study participants, we asked each of them to collect a stool sample each day over the duration of the workshop, and then to mail a stool sample 1 week after the workshop ended. Through this design, we combined methods from metagenomics, computational biology, and cultural anthropology to seek to conduct a holistic analysis of the linkages between fermented foods, local environment, and public health.

Our goal in collecting qualitative anthropological data was to relate the stories and the practice that fermentation revivalists carry with them to the microbiology we would detect later. From this perspective, every family recipe and kitchen improvisation is a step toward shaping microbial biodiversity in our foods and in our own bodies. Every cheese cave, wine valley, and cabbage patch likely has its own collection of microbes, to say nothing of our kitchens and stirring spoons. After transcribing interviews and uploading field notes into QDAMiner, we identified a number of inductive and deductive themes that we will explore below.

The workshop created an educational space apart from microbiopolitical food safety regulation, catering to an educated group of fermenters eager to similarly claim expertise within a range of sensory, scientific, and culinary bodies of knowledge. Unsurprisingly, as Katz’s bookshelf featured anthropological work including Paxson’s [25] The life of cheese, Katz and workshop participants rejected the Pasteurian logic of food regulation in favor of actively shaping a microbial landscape that was influenced by a larger socioecological landscape. During the first day, several participants asked how best to avoid harmful bacteria or contamination, questions motivated by living within the larger US and Canadian regulatory system that polices bacteria. Explicitly influenced by Paxson, Katz deconstructed these assumptions, explaining “there’s not a registry of good and bad bacteria…we ultimately don’t know enough about microorganisms to make these moral judgements.” Rather, he described fermentation as a means for shaping a particular community through different pushes and pulls of acidity, vegetable matter, and salinity. “Of all the communities of microorganisms, the question is which will develop?” he continued. Conceived as such, the practice of fermentation is thus a practice of creating different landscapes, what Katz called “manipulating environmental conditions” to make a fermented food amenable to acidic, salty, hot, or ammonium-rich bacterial communities.

Workshop participants seized on this heuristic of shaping environments as they reflected on their experiences with fermentation during interviews and participant observation. Maya, a trained cook and fermentation entrepreneur, spoke specifically about interacting with microbial environments. “I don’t really do anything,” she explained, contrasting her experience as a high-end chef to her new work as a fermented food seller decentered from the creation of her products. “I mean, I’m not making the vegetables ferment. I’m just creating an environment where that will happen. You know, I’ve learned along the way certain things to make sure that I have a better result, but I’m not actually fermenting things…I set it all up and I step out of the way.” No longer a cook as such, Maya describes her work in terms of being an environmental steward. Carl, a Midwestern IT professional, similarly referenced letting the fermented environment work to cultivate unique, strong flavors at the microbial level that are otherwise absent in the larger food system. “We can introduce a lot of umami flavors, it seems like…that’s part of the funk that develops,” he explained. This search for distinctive tastes differs from the nationalist discourses around fermentation described above in that Carl is not recreating family or place-based recipes so much as chasing the byproducts of this microbial ecology. “In all these ferments there’s the souring that happens through the production of lactic acid. Some people can taste the difference between lactic acid and acetic acid, and I can, and I prefer the lactic acid.” Carl, who distinguishes between the vinegary taste of acetic acid and the sharper “funk” of lactic acid, takes pride in the ways that he has learned to shape the distinctive variations in his food. Although he references protein structures and glutamate compounds in our discussion, Carl’s definition of a successful ferment leans more on sensory experiences of taste and touch to guide the ferments that he creates.

While all the fermenters referenced microbes in our interviews, most described fermentation as part of a larger set of environmental practices including gardening, foraging, or simply walking in forested spaces. Maya, who grew up eating fermented food, began making fermented products after learning to have “a conversation with plants. And that was so exciting for me to, like, meet the neighborhood go around and spend a lot of time on the trails…and then as a chef you get knowledge of plants and you’re like ‘Okay – how do I eat you?’ Or, what medicine are you. What’s your power, what’s your personality?” Similarly, Karen, in the early stages of starting a fermentation business, explained “I started looking at how I could value the marginal, like the weeds in my garden. Instead of ripping them out. And so we started playing around with dandelion, and nasturtium, and calendula marigold, and infusing those into our krauts…So we thought between the wild fermentation and the wild edibles, lets market ourselves as this business that helps you re-wild yourself and get back in touch with nature.” Every member of the workshop took pride in gardening or growing foods as a way to resist homogenizations of flavor or in the experience of eating. Maya’s idea of meeting the neighborhood and Karen’s hope that fermentation could help her family and her customers “re-wild” themselves speaks to the larger ways in which fermentation is helping this community embrace a place-based knowledge and praxis. All but two fermenters mentioned that fermentation has entered their lives along with small-scale vegetable cultivation and foraging, particularly growing cabbage that can be used for sauerkraut or kimchi.

Workshop participants described how these small changes to the landscapes where they live influenced their fermentation, while Katz reminded us they are part of the story of heritage fermentation as well. A few hours into the workshop, Katz drew our attention to the ecological constraints within a larger landscape that would influence the possibilities for a microbial landscape. “You know the famous Belgian open fermented beers,” he told us. “Where that happens is in a valley that was once dominated by cherry orchards. So if you have a concentration of a certain kind of agriculture in the geographical area that would certainly have implications for the density of microbes in the air, the distribution of what kind of microbes you find in the air…and then I think that that’s definitely an aspect of terroir that people are talking about more and more.” Where some commercial food suppliers leverage local microbes as a scientific marker of terroir [26, 61], the participants in this workshop saw microbial terroir as a means to an end featuring creativity, flavor, and distinction in an alternative food system. “The first time I made kraut I remember moving my body,” explained one participant, “squeezing the fruits, the vegetables, it’s like a work out in a really nice way…the physical component of it is just really important to me to feel more connected to the food.” Terroir as such is a means to an end, not a marker of high-end cuisine or geographic distinction in a market but a result of a locally situated authenticity. As Paxson and Helmreich [31] argue, microbes in this context provide a way to think through larger sociopolitical relationships between people, place, and the food system. In particular, fermentation as a skill rediscovered or reaffirmed in spaces like these workshops help to support a body of knowledge and practice where participants feel greater control and agency over the foods they eat and the spaces where they live. Kelsey, who came to fermentation after seeking to rebuild her gut microbiota, sees the creative possibilities of learning to ferment as a means to build ecological knowledge. “It’s amazing that we’re in this period of time when people can reach adulthood with such a limited skillset, or zero skillset,” she laments. Her enthusiasm for fermentation has led her to both new foods and new medicines as she explores non-pharmaceutical and plant-based medical traditions.

Warren was not alone in these sentiments. Several other participants and Katz himself contrasted the diversity of flavors and knowledge of local and fermented foods with a larger homogenization in a global food system. Signaling cooperative and anti-establishment politics in American Left and Green circles [39], the workshop space featured counter-culture books, zines, and artwork lamenting corporate control in industrialized agriculture. Like Warren and Kelsey, Katz placed the practice of fermentation within a larger critique of a Pasteurian state that welcomed industrialized agriculture and criminalized local and microbially variable food production. “I feel like, here we are among this population of de-skilled, infantilized people, and you know food is just food – it’s this transaction at the supermarket. And depending on how much money you have in your wallet you have more choices, but I just feel like food is so much deeper than that.” It is beyond the scope of this paper to review the scholarly literature on the ways in which food is and is not a capitalist commodity [76‐79], but ethnobiologists and agrarian studies scholars recognize the transformative effects of practice on knowledge and identity [80, 81]. Fermenters were keenly aware of the need for knowledge-sharing spaces like this workshop to structure the transfer of knowledge and microbial cultures. While all in attendance had read at least some of Katz’s books early in their experience, most mentioned informal networks that allowed them to swap recipes, find community, and, importantly, share microbially rich cultures that could be used as starters for fermented foods like yogurt, sourdough bread, or kombucha. As living gifts, these fermented starters share qualities with seeds, or plant starts studied by ethnobiologists [34, 82], sustaining not just a food product but also a social relationship.

In addition to distinctive carriers of place, flavor, and skill, several fermenters used the workshop to embrace the healing potential of a balanced microbial ecosystem. Four told stories in which fermented foods were central to their experiences of living with chronic illnesses, including cancer, HIV, and severe gastrointestinal distress. Warren, a cancer survivor, explained that he first encountered fermented foods by looking through peer-reviewed literature on probiotics, particularly kombucha. “Yeah when the cancer thing happened, I'm the type of person where I’m kinda all in. Alright, okay, let’s fight this right?” Later, he continued, “I probably drink 7-14 ounces at least per day.” Fermenters who looked to these foods for health did so within a larger dietary context of promoting some kind of healthy gut flora in their own bodies. Although many had read medical reports on the microbiome, none articulated specific probiotic or prebiotic genera that they hoped to introduce into their bodies. Rather, they came to imagine some microbes as allies in their fight to stay healthy and others as impediments. “I know we can’t put it into good and bad like that, but you can turn a dis-biotic situation into a balanced situation,” argued Kelsey. “I probably took antibiotics, the five day Z packs [azithromycin], twice a year every year,” she continued. Kelsey blames this childhood exposure to antibiotics for chronic bowel problems, a condition that led her first to read Weston Price’s [83] early work on comparative nutrition and later to literature on fermentation and the microbiome. Like Warren, she pursues fermentation not necessarily because it provides a specific healthy bacterial genera but because she wants to create a healthier environment within herself where her gut flora can flourish. “So you arrived to adulthood and you have these problems but it's not mysterious…it's like going to battle, you kill first and then you have to regenerate. And I did that with bone broth and with fermented foods.” Both Kelsey and Warren used military language to describe how specific fermented foods provided microbial allies for their bodily ecosystems, noting their frustration with conventional medical approaches that favored chemotherapy and antibiotics, respectively. More generally, fermenters named benefits including clearer skin, regular bowel movements, stronger immunity to seasonal illnesses, and improved energy throughout the day. “There’s literally a quickening, you feel yourself coming alive from the inside out. And then you start to seek those foods out,” explained Maya. Coming alive, which Warren also described, is a function of how fermenters imagine themselves to be reshaping their bodies through the live microbial cultures of their fermented foods.

Both implicitly and explicitly, the creative and engaged changes that fermenters experienced as they learned to make fermented foods then manifest in how fermenters imagine themselves to cultivate the microbial communities within themselves and their foods. Over the course of our interviews and participation in the workshop, the fermenters discussed questions of health, place, and creative labor on scales ranging from fermenting crocks to farms. In agrarian studies and ethnobiology scholarship [1, 13, 84], landscapes are assumed to be in dialectic relationship with the cultures that manage them. There are no farms without farmers, and local cultural knowledge or norms relating to that natural resource management goes on to create new habitats for human and non-human life. However, the innumerable dietary and lived confounds in the human body, as well as the difficulty in studying how fermented foods impact the gut microbiome in the places where they live and eat mean that we cannot assume that the same dynamics work the same way in our fermented foods. To test what sorts of microbial ecologies fermenters created when they made these foods, as well as how those ecologies interacted with human bodies, we conducted a series of microbiological and genomic analyses.

In total, we identified 6923 ASVs from the 82 samples that passed quality control. The 40 food samples contained 1595 ASVs, and we identified 6067 ASVs in 42 fecal samples. Of the 6923 ASVs, 605 were shared between the food and fecal datasets. Both food and fecal samples were dominated by a small number of phyla. The fecal samples were dominated by Bacteroidota, Firmicutes, with lesser contributions of Proteobacteria, Actinobacteria, and low-abundance phyla (Fig. 1a). The food samples contained predominantly members of the Firmicutes and Proteobacteria (Fig. 1b). At the generic level, most food samples were represented predominantly by a small number of high-abundance genera, predominantly lactic acid bacteria and Gammaproteobacteria (Lactobacillus, Lactococcus, Leuconostoc, Pseudomonas, Weisella, Yersinia, Bacillus, Acinetobacter, and Pantoea) (Fig. 2). In total, we identified 226 different variants of lactic acid bacteria in our food samples, 90 of which belong to the genus Lactobacillus. In contrast, the microbial communities of the fecal samples generally were less dominated by high-abundance genera, with Bacteroides, Faecalibacterium, Parasuterella, Phascolarctobacterium, Prevotella, and Catenibacterium being the most common taxa (Fig. 2).

Beta diversity ordinations indicated a clear and significant separation (PERMANOVA: R² = 0.204; p < 0.0001) in the food and fecal microbial communities (Fig. 3, top left) along the first dimension. Food samples clustered into distinct communities (PERMANOVA: R² = 0.325; p < 0.0001) corresponding with the five food categories listed in Table 1 (Fig. 3, top right). The final tempeh sample (24-h fermentation) and the two yogurt samples plot as outliers from the other members of their corresponding food categories. Bacterial communities within the fecal samples (Fig. 3, bottom) clustered tightly by individual (PERMANOVA: R² = 0.805; p < 0.0001). The chronological order of the fecal samples was not significantly associated with fecal beta diversity (p = 0.197). Along the first dimension there was a clear separation between one individual, Fermenter 6, and the other members of the workshop, and in general, beta diversity was evenly spread along the second dimension. This separation may be explained by a difference in relative fermentation experience or medications taken between Fermenter 6 and the others.

From the 605 ASVs shared between food and fecal samples, we identified 25 candidate ASVs that are suspected to have been transmitted from fermented food samples to the gut microbiomes of the workshop participants (Table 2). Seven of 25 ASVs were from the genus Lactobacillus, followed by 2 each of Bacillus, Lactococcus, Leuconostoc, and single representatives of 12 other genera. In three cases, we were able to identify these ASVs to the species level (Bacillus cereus, Lactobacillus paracasei, and Lactobacillus curvatus).