The environmental
microbiome

What is the environment?

Although not in the context of human health, Winogradski’s environmental microbiology in the late 1800s brought forth ideas of the interconnectivity of microorganisms in natural environments such as soil and highlighted diversity and ecological understandings of microbiology.

Contemporary research on the human gut microbiome follows a similar interest in this interconnectivity and seeks to understand how the "environment" influences the development and characterization of microbiomes.

But how do scientists attempt to define the environment and its impact on the microbiome? What are the implications of the way the environment is understood? And what are some STS/anthropological perspectives on these definitions in practice?

Broadening the Meaning of Environment in Microbiome Science

Exposome Research

Some scientists have moved beyond the term environment and instead utilize an "exposome" based framework. This attempts to consider the total multi-faceted environment that is dynamic over a life course and recognizes not simply pollutants or diet, but also the influencing factors of socioeconomic status and structural conditions (Renz et al. 2017).

While attempting to study everything all the time seems like quite a massive venture, some scientists are drawing upon chemistry to identify new molecules that are part of exposomes and some are utilizing bioinformatics to make sense of interactions of microbiome data (genomics from samples) with exposome data (collected from wearable sensors that measure chemicals and microbes in the air).

The important conclusions that can be drawn from exposome data is summarized by De Wolfe et al. (2021). Building on discussions of space, geography, and social/spatial inequalities, the question emerges as to “what environmental factors—animals, spaces, habits, lifestyles, migrations, food, agricultures, abiotic forces, chemical exposures and disease prevalence, known collectively as the exposome—lead to differentiation in the human microbiome and what are the implications of this differentiation for society, politics, and governance?... For example, human microbiomes can hold traces of living conditions (the exposome) which can in turn inform questions of inequality and social (in)justice…”

One Health

In this research framework, the environment is classified as the non-human and the non-animal yet the interconnectivity between environment/human/animal is of focus.

In microbiome research with the One Health framework, the microbial transfer between these three spheres is studied. Methodology includes software analyses of longitudinal data sets to uncover patterns in direction/magnitude of transfers and effect of external influences on a microbiome’s stability, composition, and function (Trinh et al. 2018).

Within this research field, a key direction is that of antibiotic resistance, where the transfer of Antibiotic Resistant Genes (ARGs) is explored and the gut microbiome of humans and animals becomes a key site for this transfer from environmental sources of ARGs.

When the Environment Gets Too Broad...

We've seen how frameworks such as the exposome seek to broaden the factors included in "environment" to emphasize more holistic and structural conditions that may influence the gut microbiome.

But some research directions navigate in a different direction - using the uncertainty of the definition of "environment" to problematically conflate specific attributes with groups of people.

This is seen primarily in population-based microbiome research. For example, the “environment” becomes conflated with “modes of subsistence” and “lifestyles” (i.e. “uncontacted”, “rural”, “traditional”, “urbanindustrialized”), which are both directly connected to dietary patterns. This is complicated by many articles that write “diet and environment”, implying two separate concepts yet still are written as interlinked. Additionally, the "environment" also becomes associated with infrastructure (ex. sanitation systems) without recognizing the sociopolitical forces that influence these conditions. In studies that investigate antibiotic resistance in microbiomes, the “environment” becomes a possible source for the origins of ARGs (through horizontal gene transfers between bacteria and their environment), in problematic linkages that rely on images of the "uncontacted" tribes who have ARGs in their microbiomes and conclude that these groups must have acquired them from the environment.

These assumptions and conclusions seem to rely on environmental determinism which Stallins et al. (2018) describe as the ways in which some microbiome research maps the environment onto human bodies and defines them according to these constructed environments. They write that on one hand this could "encourage a greater awareness on how microbial environments matter and how they might be altered to address health disparities related to malnutrition, physiological and psychological stress, and pollutant exposure". On the other hand such determinism might only reinforce stereotypes of race and class as environments become defined in bodies as "biomarkers".

Hobart and Maroney (2019) extend this critique of the conceptualization of the environment in microbiome research, especially studies that investigate ancestral microbiomes through the microbiomes of contemporary Indigenous groups. They write that: “by drawing explicit connections between Indigenous environments and Native bodies and suggesting that these fundamental links offer some kind of key or answer to the maladies of those who, as modern subjects, do not hold those same originary relationships to place.”, in essence problematically equating entire communities with geography and "lifestyle patterns". These racist sentiments of Indigenous peoples as closer to nature/their environment become extractive in the context of microbiome research with goals of therapeutics for “Western” diseases.

Perspectives from
STS & Anthropology

The Environment Multiple

Some scholars such as Benezra (2021) have identified the utility of such a broad and changing definition of environment. She writes: “The lability of environment in microbiome science makes flexible concepts of bodies, kin, exposures, and sociality—and what value there is for different actors to concretize different meanings." For example, in her observations of a microbiome research lab, participants (mothers from Bangladesh) and scientists each understood the environment differently - "Study mothers focus on pathogenic microbes, think about generations of family, define environments as house, market, bodies, food. The Gordon Lab focuses on microbes as evolutionary kin, define environments as genetic, intestinal, geographic." She concludes that “Microbiomes are environments of this multiple kind, circulating and confounding the inside of bodies, the outside world, and back again…I see microbial kinships as bio-socio-enviro-exposo amalgamations, not separate from the science that defines microbiomes, voids structural contexts, helps and harms." The fluidity of the term "environment" thus allows it to move within the networks of relations of microbiomes and take on subjective meaning to the variety of perspectives that draw upon it.

Environmentality

What distinguishes an organism from an environment? Formosinho et al. (2022) attempt to address this question with their concept of environmentality, which envisions a framework of shifting, fluid, perspectival relations with no fixed or external concept of "environment".

While this paper does not critique the use of "environment" in microbiome research, it presents a useful new framework that could help critically analyze certain vague and flippant uses of ‘environment’ in microbiome research. For example: the study by Conteville et al. (2019) showed that the microbiomes of Yanomami people from Brazil had an abundance of genes for cobalt, cadmium, and zinc resistance but the authors dismiss this finding on the basis that “cadmium contamination may occur as a consequence of the continuous discharge of batteries anywhere by the Yanomami along decades.”. Might the framework of environmentality be applied to research such as this to elucidate the complex networks of power, politics, mining practices, pollution, toxicity, and activism that extend the concept of ‘environment” beyond the bodies of those humans being studied and their immediate environment

references

Benezra, Amber. 2021. “Microbial Kin: Relations of Environment and Time.” Medical Anthropology Quarterly 35, 4: 511-528. DOI: 10.1111/maq.12680.

Conteville, Liliane Costa et al. 2019. “Gut Microbiome Biomarkers and Functional Diversity Within an Amazonian Semi-Nomadic Hunter– Gatherer Group.” Frontiers in Microbiology 10:1743. https://doi.org/10.3389/fmicb.2019.01743

De Wolfe, Travis J. et al. 2021. “Chasing Ghosts: Race, Racism, and the Future of Microbiome Research” mSystems 6: e00604-21. https://doi.org/10.1128/mSystems.00604-21

Formosinho, Joana et al. 2022. “Environmentality in biomedicine: microbiome research and the perspectival body.” Studies in History and Philosophy of Science 91: 148-158.

Hobart, Hiʻilei Julia and Stephanie Maroney. 2019. "On racial constitutions and digestive therapeutics." Food, Culture & Society, 22, 5: 576-594, DOI: 10.1080/15528014.2019.1638120

Renz, Harald et al. 2017. “An exposome perspective: Early-life events and immune development in a changing world.” Journal of Allergy and Clinical Immunology 140, no. 1: 24-40. http://dx.doi.org/10.1016/j.jaci.2017.05.015

Stallins, J. Anthony et al. 2018. "Geography and Postgenomics: How Space and Place are the New DNA.” GeoJournal 83: 153-168. https://doi.org/10.1007/s10708-016-9763-6

Trinh, Pauline et al. 2018. “One Health Relationships Between Human, Animal, and Environmental Microbiomes: A Mini-Review.” Frontiers in Public Health 6:235. doi: 10.3389/fpubh.2018.00235