The dawn of ethnomicrobiology: an interdisciplinary research field on interactions between humans and microorganisms

Ethnobiology is a field of research that encompasses complex bodies of knowledge, cosmologies, actions, and interactions between people and biodiversity, operating at the intersection of several scientific disciplines that address both cultural and biological issues. It therefore involves the study of highly diverse, dynamic, and historical relationships between people, biota, and environments [1,2,3]. To date, much of this research has focused on terrestrial vascular plants, macromycetes, vertebrates, and insects. However, there is increasing interest in traditional knowledge related to other taxonomic groups that contribute to biodiversity and their interactions with cultural diversity [4, 5]. One of the central goals of ethnobiology is to integrate knowledge systems from diverse stakeholders, which is especially relevant when addressing socioecological challenges [6]. As a result, this interdisciplinary approach has evolved through different epistemological frameworks and historical stages [2,3,4,5,6].

Ethnobiology has been shaped by diverse biological perspectives, with integrative strategies related to knowledge systems varying across cultures worldwide [7,8,9,10]. Historically, attempts to explore the complex relationship between biodiversity and cultural practices have often focused on specific taxonomic groups. Ethnobotany, for example, focuses on human-plant interactions [7, 11, 12], while ethnozoology focuses on human-animal relationships [13,14,15,16,17]. Although less studied, organisms such as fungi (especially macro fungi) have also been studied by ethnomycology, which examines their role in food, medicine, recreation, and household economies [18, 19].

In contrast, the relationship between humans and the microbial world has received relatively little theoretical attention, even though microorganisms are the earliest and most diverse organisms on the planet. Microbes play a critical role in human food and health systems, and their activities and byproducts are often experienced through smell, taste, texture or other attributes. Throughout Earth's history and the development of civilizations, a complex, multilateral relationship has developed between humans, the environment, and microbial communities [20]. Despite their vast diversity, microbes have been largely overlooked in ethnobiological studies, even though they are integral to the ecological interactions that many ethnobiologists study.

The term “ethnomicrobiology” is rarely used in scientific literature, and evolutionary ethnomicrobiology has yet to be formally established. The term was first introduced by Souza [21] in a study of traditional agricultural practices in Mexico, where local people from Puebla and Morelos managed Phaseolus species and their associated Rhizobium bacteria. These authors found that farmers were aware of how their practices positively affected soil microbial communities and crop yield, drawing attention to an often-overlooked aspect of ethnobiology. Subsequently, Tamang [22,23,24] defined ethnomicrobiology as a field focused on understanding the indigenous knowledge used to produce culturally and organoleptically acceptable fermented foods through natural fermentation. However, this definition may be too narrow, given the wide range of processes involving human-microbial interactions. Other authors have proposed the term “ethnozymology” to describe the science of fermentation in traditional diets, emphasizing the integration of Traditional Ecological Knowledge (TEK) into fermentation practices, using native, autochthonous microbiota from plant ingredients and other natural sources [25]. This approach highlights the role of TEK in guiding the dynamics of microbial communities associated with fermented products. However, these concepts may be limited when considering the full range of human-microbe interactions.

The primary goal of this work is to review the existing literature on the diverse range of human-microbe interactions, in order to establish ethnomicrobiology as a cohesive field that unifies concepts and develops theoretical and methodological frameworks for studying these relationships. We aim to contextualize the historical and dynamic interactions between microorganisms—whether at the level of population, community, species, or strain levels—and human activities. As an interdisciplinary and transdisciplinary field, ethnomicrobiology incorporates multiple theoretical and methodological perspectives to study the relationships between microorganisms (including bacteria, viruses, fungi, and archaea) and human cultures (Fig. 1). We recognize the critical role that microorganisms have played throughout human history and their ongoing influence in areas such as food, health, and various production systems. This approach provides ethnobiologists with valuable research tools to analyze how different cultures perceive and interact with microorganisms, how microbial communities are conserved, maintained, and utilized in different contexts, and how these interactions shape the interplay between the micro and macro worlds.

Fig. 1figure 1

Ethnomicrobiology is an interdisciplinary and transdisciplinary field that bridges ethnobiological studies (red color below) and microbiological sciences (yellow color above). Rather than being treated as an independent branch of ethnobiology, ethnomicrobiology requires the collaboration of various biological and social sciences to unravel the complex and intricate effects of human-microbial interactions (all the colors in between the coalition of major disciplines). We envision ethnomicrobiology as a vibrant, woven textile, where different disciplines intertwine to propose a unified concept and diverse perspectives on human-microbe interactions across ecological, cultural, economic, functional, evolutionary, chemical, and other approaches. This emerging field and all the perspectives involved allow us to rethink the historical and dynamic relationships between microorganisms and human activities in a myriad of ways (Image by Alejandra Cruz Rodriguez)

Ethnomicrobiology is based on the ethnobiological goal of understanding and reflecting on local knowledge about microorganisms and the products that result from these interactions. The emerging ethnomicrobiological framework seeks to recognize and value the skilled individuals who manage the invisible microbial world, whom we will refer to as microbial managers. It also seeks to move beyond stereotypes that frame indigenous peoples’ knowledge of biotic relationships as primarily visual and to open new ways of exploring biodiversity through other senses.

In this work, we explore the global developments and trends in ethnomicrobiology. This review offers a novel and original perspective that addresses the emerging growth of this field within the ethnosciences and its future directions. We conducted a systematic review of scientific journals, books, and book chapters that address human practices or traditional knowledge in the management of microbial communities in soil, fermentation, and health. We include peer-reviewed works of qualitative and quantitative research, reviews, and dissertations. We also include studies from the last 30 years, unless older studies are foundational or critical for the review. We limit our search to studies published in languages not covered by the research team's language skills, opinion pieces, letters to the editor, or non-peer-reviewed articles. Our search included articles from international databases such as Web of Science, Scopus, Google Scholar, PubMed, and specific journal websites. We focused on terms related to ethnomicrobiology, ethnozymology, fermentation, traditional knowledge, microbial management, fermentation and cultural practices, and microbes.

In this review, we emphasize the implication of ethnomicrobiology in shaping both microbiological and ethnobiological research agendas. The following sections explore a wide range of activities that involve intentional human-microbial interactions, including practices designed to preserve, promote, maintain, or eliminate microbial groups. These practices encompass food preservation techniques such as fermentation, pickling, drying, salting, and smoking, as well as practices intended to avoid microbes, such as tanning. In addition, we will examine microbial management activities in soil, including agricultural practices, composting, and geophagy. We also discuss the role of microorganisms in traditional and folk medicine, where microbial management is integral. In addition, we highlight the relevance of ethnomicrobiology to evolutionary studies, particularly by integrating microbial research trends with evolutionary frameworks such as the domestication of microbial fermentation environments, niche construction, and the co-evolution of microbes with domesticated plants. Finally, we address the social-critical dimensions of ethnomicrobiology, emphasizing its importance for understanding broader societal and ecological dynamics.

The relevance of ethnomicrobiology to the microbiological and ethnobiological research agenda

Do humans have microbial blindness, or do we rely on visual cues to the detriment of our other sensory data collection? Certainly, we live in a microbial-dependent world; without microbes, important geochemical cycles such as those of nitrogen, carbon, and phosphorus would collapse, decomposition would stop, and no animal (including humans) would be able to produce and digest its food, and life as we know it would truly cease to exist [26]. It is common for many people to associate microorganisms with agents that cause diseases in plants and animals. However, throughout history, humans have used microorganisms for a wide range of activities. Our relationship with these diverse organisms is both intimate and vital, affecting various aspects of our daily lives, including functions of which we are often unaware [27,28,29]. The formal study of microbial communities only began after technological advances in microscopy and the pioneering work of scientists such as Koch, Pasteur, and De Bary in the late nineteenth century. These advances stimulated interest in microbiology as a scientific discipline. However, long before microbes were understood, human cultures around the world engaged in activities such as salting, smoking, roasting, lyophilization, nixtamalization, tanning, and fermentation of foods, beverages, and dyes, all of which involved microbial management processes [30,31,32,33,34,35,36,37].

Microbiology is the study of microscopic organisms, including unicellular, multicellular, or acellular forms [38, 39]. It includes both eukaryotes, such as fungi and protists, as well as prokaryotes, viruses, and prions. Although prions and viruses are not considered living organisms in the strict sense, they are part of the microbiological agenda. Microbiology also serves as an umbrella for several subfields, including virology, mycology, parasitology, bacteriology, immunology, and zymology, all of which study different aspects of microorganisms. The interactions between humans and the microbial world have revolutionized life, particularly in medicine through the use of antibiotics, and vaccines, reducing the incidence of infectious diseases [40, 41] (in Fig. 1, related disciplines of microbiology shown in yellow). Microbiology has also made significant contributions to fields such as environmental management, genetics, and molecular biology (in Fig. 1, related disciplines of microbiology shown in green), but perhaps its most profound impact has been in food production and biotechnology, evident in the wide range of products such as wine, bread, and cheese, among others [42,43,44].

Despite significant advances in microbiology, the vast empirical knowledge of microbial processes held by traditional societies has often been overlooked. Microbes have been understood and managed in all human cultures for centuries [45]. Many communities engage in agricultural and culinary practices that directly shape microbial communities in both soil and food [46, 47]. The diversity of fermented foods resulting from these practices is critical not only for human nutrition but also as a form of cultural expression [48]. Moreover, these interactions extend beyond food, encompassing traditional health practices, which often involve microbial activities [48]. A deeper understanding of local knowledge systems related to microbial management may reveal microorganisms as an integral part of local biodiversity with significant health benefits.

One approach often used by ethnobiologists is the biocultural perspective. If we consider biodiversity to include the vast diversity of microorganisms, it becomes crucial to recognize these microorganisms as agents that establish relationships with human groups and cultures. Integrating these biological entities into ethnobiology has significant implications, especially since human interactions typically involve entire microbial communities, populations, strains, or even entire microbial ecosystems, rather than just individual species. While there are prominent examples of interactions with specific microorganisms, such as those used in beer production or the use of Aspergillus in cheese-making, these relationships often reflect broader ecological dynamics that involve multiple senses and extend beyond mere visual perception. Understanding our relationships with microorganisms requires attention to these multisensory interactions. In addition, the management and production of artifacts to manipulate microbial groups play a critical role in this complex web of interactions between living organisms, objects, and humans [49].

Incorporating microbiology into ethnobiology is critical for understanding ecological knowledge, cultural meanings, and the sustainable management of microbial biodiversity. It also provides insights into how human actions shape microbial communities and influence selection or domestication processes that favor certain microbial groups over others. In addition, studying the effects of human management on plant and animal microbiomes highlights the interconnectedness between macroorganisms and microorganisms. Ethnomicrobiology also opens discussions on ethical issues such as the use of microorganisms, bioprospecting, biopiracy, and intellectual property rights. Moreover, it serves as a reminder that we live in the “Microbiocene”, an era in which we must acknowledge our dependence on these organisms, even if we often experience them primarily through their “osmocosm” (the scents of the universe) [50].

Identifying activities that involve deliberate actions on human-microbial interactions

Historically, ethnobiological studies of plants and animals have explored a wide range of topics, including behavior, use, cultural transitions, social relationships, and their ecological and evolutionary implications [7, 51]. Plant and fungus collectors, managers, and domesticators possess extensive knowledge of the taxonomy, biology, and ecology of these species, just as hunters, ranchers, and breeders do for animal groups [17]. Local experts play a critical role in preserving and transmitting ecological knowledge about human interactions with biota [52, 53]. Similarly, people around the world engage in a variety of practices to manage microbial communities. Whether to maintain, promote, restrict, or eliminate them, these human practices represent diverse forms of microbial management (Fig. 2). Today, different cultures have different relationships with microorganisms, which we will outline in the following section.

Fig. 2figure 2

Activities that involve microbial management. Fermentation is a universal process used to produce foods, beverages, dyes, and other products. In these processes, specific microbes are managed and selected to produce desired products, while other microorganisms that may cause spoilage are intentionally avoided. Preservation practices involve physical methods such as drying, smoking, salting, and tanning to restrict microbial communities that could lead to spoilage. Soil management practices are widely used around the world, to encourage beneficial microbes that improve soil health and ultimately agricultural yields. On the health front, many diseases are linked to imbalances in the microbial communities within the human body. Folk and traditional medicine has long employed practices to maintain balance within these communities. In addition, the increase in health concerns in recent years has highlighted the importance of a healthy diet, particularly the consumption of fermented products, in maintaining microbial balance. (Images created using Copilot in Windows AI)

Fermentation for food and beverages

Fermentation is perhaps the most tangible and oldest technique that allows humans to perceive and interact with the microbial world in their daily lives, even without seeing the agents responsible for this transformation. Fermentation is a metabolic process carried out by various organisms to produce energy. Microbial groups such as bacteria and yeasts convert organic compounds such as carbohydrates through enzymatic reactions (mainly in the absence of oxygen) into simpler molecules such as alcohol or a wide variety of organic acids [54, 55]. Fermentation has been used as a common process in the production, preservation, enhancement, and transformation of various foods and beverages [54, 55]. However, other products such as textiles, dyes, compost, and many other common commodities undergo fermentation processes [56, 57]. In the food industry, fermentation has facilitated the increasing production and diversification of foods and beverages; in fact, it is estimated that approximately an average of 50–400 g per capita of fermented foods and alcoholic beverages are consumed daily worldwide, accounting for approximately 5–40% of the total daily food intake by humans worldwide [58,59,60,61]. These products are not only essential to the human diet but have also played a historically significant role in shaping the socio-economic, cultural, and identity aspects of human life [59, 62,63,64]. Thus, these products should not be considered as commodities alone, but as part of the complex cultural contexts in which they are embedded.

Microbiological studies have generally assumed that traditional fermentations capture wild and mostly uncontrolled organisms, resulting in heterogeneous and unpredictable outcomes for biotechnological purposes or even products that may endanger human health [65]. However, several studies have documented complex knowledge systems by which people manage the effects of such heterogeneity through practices such as controlling the room temperature, covering the fermentation containers, adding specific plants that contain enzymes for food fermentation processes, or as other sources of more specific microbial communities [66,67,68]. In addition, some producers have conditioned or constructed specific fermentation rooms, containers, and other facilities that play an important role in promoting the collection of microbial communities and other practices that help maintain them by avoiding cleaning chemicals and soap [69, 70].

Fermentation can be accomplished using inoculants, also known as starters or starter cultures, which are established microbial consortia added to initiate, enhance, or drive the fermentation process [71,72,73,74,75]. Similarly, backslopping is the practice of using a portion of a previous batch of fermented food or beverage to inoculate a new batch. This is commonly done in processes such as sourdough bread making or yogurt production [76, 77]. The purpose is to inoculate an old batch to start the fermentation process with new substrates by introducing those beneficial microorganisms from a previous batch [

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