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Research on the microbiome is challenging long-held assumptions about human health. These claims are forcing biologists to fundamentally reconsider what it means to be human in a microbial world. This article surveys and addresses the ontological and anthropological claims associated with microbiome research in an effort to answer the question, ‘what does it mean to be a human created in the image of God in light of the microbiome?’ Specifically, this paper accounts for the claims of microbiome research by adapting an existing model of theological anthropology from the work of Dietrich Bonhoeffer. This model accounts for both the current and future state of microbiome research as well as the claims associated with increasingly popular “mega-organism” or holobiont models of human personhood, by defining the imago Dei as interpersonal and inter-person relationality, as opposed to a fixed set of attributes rooted in the human mind or will. Rev. Aaron M. Hill is the Production Editor for VII: The Journal of the Marion E. Wade Center and holds an M.A. in Systematic Theology (2019) from Wheaton College in Wheaton, Illinois and an M.A. in Christian Education (2007) from Southwestern Baptist Theology Seminary in Fort Worth, Texas.

In 1822, Alexis St. Martin was “accidentally wounded by the discharge” of a musket at a military outpost in Michigan Territory.1 The blast struck the fur trapper from behind, blowing a hole through his chest cavity.2 Army surgeon William Beaumont pushed portions of the fur trapper’s lung and stomach back into his chest, “as far as practicable.”3 Miraculously, the wounds healed and St. Martin went on to live a long life; however, the incident permanently fused his stomach wall to his chest. Through this “orifice” Beaumont performed experiments on St. Martin’s digestive system over the course of several years.4 First published in 1831, these experiments formed the foundation for gastroenterology in the twentieth century. One of Beaumont’s most prescient findings was that his patient (victim’s) mood was linked to the rate of his digestion, specifically his “fear and anger.”5

What neither Beaumont nor gastroenterology in the twentieth century understood was the role microbes play, not just in the gut but throughout the whole human body. For many decades two paradigms prevented this microbial insight. First, modern medicine revolved around an “us-versus-them mentality,” pitting microbes against flourishing human life. The goal of medicine, reductively speaking, was the pasteurization of the world: “Purging … microbes and creating a biologically pure human [was] the ideal outcome.”6 Secondly, modern medicine long held that “the most important biological factor in creating a better future for humans” was the human genome.7

After almost a century of these two paradigms reigning supreme, biologists, neuroscientists, and physicians are painting a new picture of what makes human beings healthy or unhealthy.8 The discovery of a ‘missing organ,’ the microbiome, had led to an explosion of research in an effort to account for its influence on human health. This research is ushering in a new paradigm in medicine focused on “whole human care.” Biologists and evolutionary theorists are extending this new microbial paradigm beyond the health of humans to the human ‘self’—leading some to fundamentally reconsider what it means to be human.9

Being Human in a Microbial World

Two major discoveries are overturning the long-standing anthropocentric assumption that humans are “individual, discrete” organisms within a larger external ecosystem. First, research indicates that the majority (numerically) of the genes and cells contained within the human body belong to microbes. Secondly, biologists are discovering that certain aspects of cognition, the affections, the immune system, digestion, and overall health may be influenced by the microbiome. As a result, the microbiome is complicating and blurring traditional ideas of human personhood based on either fixed attributes (such as reasoning or the will) or on biological uniqueness (“the immune system, the brain, the genome”).10 The line between where humans end and microbes begin is being blurred. These findings have “profound implications…for our philosophical” and theological “comprehension of the human self.”11

Kunnen and Carlson’s 2017 article in Christian Scholar’s Review, “Deeply Connected to God’s Good World,” examines humanity’s deep connection with the “the smallest inhabitants of our world” and the need for human stewardship in the midst of a fallen world. This article will survey and address the ontological and anthropological claims associated with microbiome research, in order to offer an answer to the question, ‘what does it mean to be a human created in the image of God in a microbial world?’ This paper accounts for these claims by adapting an existing model 12 This model can account for both the current and future state of microbiome research as well as the claims associated with increasingly popular “mega-organism” or holobiont models of human personhood, by defining the imago Dei as an interpersonal and inter-person relationality—or as Steven Bouma-Prediger calls it “a being-in-relation”13—as opposed to a fixed set of attributes rooted in the human mind or will.

The Microbiome: Size and Scope

To avoid confusion, let us define some terms. In the last several decades, modern science has discovered that every human being carries on and in their body trillions of bacteria, viruses, and fungi. These microorganisms are collectively called the human microbiome. Whereas a biome describes all the life in a specific biological sphere of the earth, the human microbiome refers to all the microscopic life (“bacteria, viruses, fungi, and protozoa”) in the biological sphere of the human body.14 Within a given microbiome those microorganisms living within a “defined environment” are called a microbiota.15 The most crucial of these environments in humans, as it relates to health and personhood, is the gut microbiota.16 The vast majority of gut microbes call the colon home. Many, if not most, of the studies cited in this paper deal directly with the gut microbiota. By contrast, the model proposed in this paper addresses the entire human microbiome. In order to avoid restricting our discussion solely to a subset of the microbiome, terminology in this paper will shift between the gut microbiota in particular and human microbiome in general.

The human microbiome touches or overlaps with numerous aspects of human health and physiology. Indeed, scientists continue to uncover the extent to which symbiotic microbes living in the human colon (gut microbiota) impact everything from: (1) the immune system,17 (2) food digestion, (3) mood,18 (4) cognition,19 (5) disease processes, such as non-communicable diseases [NCDs],20 (6) and adiposity (obesity).21 Given the early state of research, it is easy to both overestimate and underestimate the role of the gut microbiota in human physiology. Specifically, it is easy to underestimate the human microbiome’s influence on capacities which “have traditionally been said to define the human self.”22 Two concrete ways to quantify the microbiome’s influence on human health are by its size and scope.

First, the vast size of the whole human microbiome is overturning the paradigm that the human (mammalian) genome is the sole driving factor in biology and medicine. When the Human Genome Project [HGP] began scientists assumed that the human mammalian genome contained up to 55,000 genes; in the end, they discovered less than half that number (approx. 22,000).23 By contrast, current models estimate that the human gut microbiota alone contains between 8-9 million genes.24 These microbes in the human gut exhibit far more genetic diversity than humans. For example, while you share 99.9% of your genes in common with every other human on earth; “any given E.coli” in your gut shares “roughly 20% of its genes” in common with other E.coli.25 In addition to genes, best estimates indicate that every human contains more bacterial cells than human cells.26 While estimates vary based on different mathematical models, and are being refined over time, the scales will likely never tip back in our favor. The cold hard reality is that you contain more bacterial cells and genes than human cells and genes. You are less You than you think.

The human microbiome, however, is not merely a hitchhiker hiding in the back of a box car—out of sight, out of mind. It is an active participant and communicant with our central nervous system (CNS) via several biochemical and neurological pathways.27 While the scope and extent of this influence is still being examined, the interaction of the gut microbiota with the CNS has profound implications for higher brain functions typically associated with free will, “self-awareness, personality traits,…[and] emotional states”—what theological anthropologists would call “the mind.” As noted previously, in their February 2018 review article in PLOS, Rees, Bosch, and Douglas argue that this research “has profound implications” for how we define “the human self.”28

Neurologist John F. Cryan and his colleagues are the forefront of this research into the microbiome and neuroscience. They note that the microbiome “influence(s) normal physiology and contribute(s) to diseases ranging from inflammation to obesity.”29 In this new paradigm “the gut microbiome plays a crucial role in host physiology.”30 Indeed, according to Cryan and his colleagues, data “suggests a role for the gut microbiota in the regulation of anxiety, mood, cognition and pain.”31 The gut microbiota communicates with the central nervous system via a pathway called the “gut-brain axis.” Along this axis bidirectional communication is mediated through several messaging “mechanisms.” Cryan and Dinan identify the currently known mechanisms of this bidirectional communication in their 2014 review paper as altered microbial composition, metabolic processes, immune system activation, and crucially the vagus nerve.

The mechanisms driving bidirectional communication via the gut-brain axis are complex and not fully understood. The correlation and/or causation between diseases and the gut-brain axis remains to be quantified and is being actively investigated through animal and human trials. To date, the vast majority of microbiome research has relied on mice; however, this research has led to an explosion of interest in the field and to the creation of several human “gut projects,” such as the American Gut Project and the British Gut Project.

The ongoing and rapid pace of research into the microbiome is constantly changing our understanding of the microbiome’s impact on human health, cognition, and behavior. The research in this article captures the state of the field in 2017 through 2018. In the last two years, new research has only reinforced the role of the microbiome with respect to human health and personhood. For example, B. B. Finlay et. al. recently proposed a hypothesis for how noncommunicable diseases (NCDs) might be communicated via the gut microbiota.32 Finlay’s proposal builds upon the work of other scholars who are actively updating Robert Koch’s postulates—a model established in 1890 for determining “whether a microbe was the cause of an infectious disease” (250). They put forward a testable hypothesis for how some NCDs, such as obesity, type-2 diabetes, and heart disease are communicated between persons via the human microbiome. The implication of Finlay’s proposal is that changes in specific microbiota, which themselves are transferrable between humans, may be able to contribute to the development of certain non-communicable diseases. If Finlay is right, then simple one-to-one disease models—where one bad bacteria or virus enters the body, is treated with a single drug, and the body returns to homeostasis—cannot adequately account for causation. These newly proposed disease models are re-evaluating Koch’s postulates through an ecological lens. As Finlay et. al. write, “we are only at the beginning of understanding the interactions within these ecosystems, the perturbations, which can be induced, and their effect on pathogen susceptibility and disease.”

The Impact of the Gut-Brain Axis

Certain bacteria in the gut produce a number of substances which may directly interact with “gut-brain signaling” mechanisms, for good or for ill. These “microbially derived molecules” interact with immune cells, such as phagocytes, in the mucous lining of the intestines.33 Some of these intermediate substances send signals from the “bottom up”—from the mucosal lining of the gut up to the brain often through the vagus nerve.34 Recent studies on these “microbially derived molecules” suggest that they are able to “cross the intestinal barrier,” enter the bloodstream, and potentially even cross the blood-brain barrier.35 Additionally, these interactions between the gut microbiota and the mucous lining of the intestines can lead to changes in pro- and anti-inflammatory compounds which “directly affect brain function,” such as cytokines. The extent to which these intermediate substances modify distinct “brain sites” remains to be quantified.36 One of the “best characterized examples” of gut-brain axis interaction occurs via the “bidirectional interaction” between enterochromaffin cells, microbes, and the central nervous system.37 These special cells are part of a metabolic pathway which plays a role in the amount of serotonin available to the nervous system, which modulates physiology and behavior.38 A breakdown in these microbially-moderated processes has been correlated and is being studied in connection with diseases such as “(AIDS)-related dementia, Huntington’s disease and Alzheimer’s disease.”39 Perhaps, most importantly, the microbiome directly interacts with the central nervous system [CNS] via the vagus nerve which conducts signals both into and out from the brain.40 This crucial pathway of communication between the microbiome and the human brain demands deeper investigation.

The vagus nerve—which is part of the parasympathetic nervous system [PSNS] and which is also part of the larger enteric nervous system [ENS]—“regulates several organ functions, including bronchial constriction, heart rate and gut motility.”41 Together the ENS and the human gut contain a massive number of neurons, even when compared to the CNS. There are 200-600 million neurons in the ENS compared to 100 billion in the CNS.42 As a result, many microbiome specialists call the CNS the “first brain” and label the nerves associated with the ENS and gut the “second brain.”43

The effects of this second brain on the first are startling. In microbiome research, scientists are demonstrating that the actions we consciously take with our first brain can alter our second brain, both in terms of the neurons in our gut and our gut microbiota. These changes reciprocally impact our first brain and our conscious or subconscious choices. Consider two heavily studied examples of this bidirectional gut-brain axis.

First, numerous research studies demonstrate that the gut-brain axis plays a key role in the relationship between obesity, diet, and food choice. 44 Conscious diet choices made with the first brain (CNS), such as chronic overeating, lead to changes in both the (2) second brain (PSNS) and (3) the gut microbiota. Specifically, vagal neurons in the gut are desensitized by chronic overeating and the gut microbiota is altered. These changes in the second brain lead to reciprocal changes in the first brain (CNS) that then play a role in conscious food choices. This feedback loop contributes to obesity, which introduces “common co-morbidities” such as heart disease as well as “deficits” in brain function like “memory, learning, and executive functions compared to normal weight subjects.”45 The feedback loop is further exacerbated by other factors such as antibiotics, either administered in childhood or consumed in low doses through meat.46 Antibiotics disrupt the gut microbiota ecosystem, eliminating species diversity and negatively impacting beneficial communities which leads to an increase in adiposity and other disease processes.47

The gut-brain axis connection extends beyond obesity, though, to aspects of cognition. Experiments with mice demonstrate that certain bacteria can “regulate emotional behavior” and stress reactions within the brain.48 Some of these effects have been replicated, albeit to a lesser degree, in a handful of human studies.49 Specific bacteria have even been identified as playing a beneficial role in human cognition and are being researched as “psychobiotics” by researchers like John Cryan.50 Experiments in mice also show that stress responses and certain behaviors can be “transplanted” from one lab animal to another via a fecal transplant (a gut microbiota transplant). These behaviors can also sometimes be “fully reversed” through an inoculation of beneficial bacteria.51 This transplantation effect has been demonstrated in lab animals to extend beyond stress responses and behaviors to aspects of cognition and adiposity (obesity).52 Crudely speaking, transplanted feces can make a skinny mouse obese in addition to making them anxious, depressed and/or ‘brave.’53 Microbiome research has also revolutionized the use of fecal transplants in humans as medical treatment. They are now used commonly to treat diseases such as IBD, C. diff infections, and are even being explored as a treatment for autism in children.54 These examples of interactions between the gut microbiota and the brain demonstrate that the microbiome plays a yet-to-be-fully-quantified role in the “neurological functions” of the brain.55 The microbiome impacts crucial aspects of human health beyond the level of relationships and stewardship, impinging on deeper ontological questions. The interdisciplinary implications of this microbiome research ought to force Christian scholars to rethink theological anthropology.

Altering Theological Anthropology

In light of this research scientists are already looking for fresh answers to the question, `what does it mean to be human?’ Indeed, many scientists are claiming that “the finding that microorganisms are a constitutive part of ourselves” means that we must develop “a new configuration of…what it means to be human….”56 They claim that we must move beyond the “idea that humans are more than mere nature,” and note that microbiome research reveals our “human and microbial worlds are inseparably ‘entangled.’” Two major paradigms that biologists have begun to adopt—in order to account for human personhood in light of a symbiotic ecosystem between mammal and microbiome—are a “superorganism” or “holobiont.”57

The first model, according to Rodney Dietert in his book The Human Superorganism, sees human beings “not [as] self-contained, self-sustaining organisms [or] pure human mammals” but as living things composed of more than one organism, a superorganism who all need each other to survive.58 Kunnen and Carlson describe this anthropological model in their article using the term “mega-organism.”59

The other frequently used term/paradigm in microbiome research is a holobiont. In this model both the “host organism and associated species” are treated “as a group” which together “serve as a unit of evolution.”60 Advocates point to the size and diversity of the microbiome compared with human mammalian cells and genes, the “highly mutualistic” relationship between the “human host” and the microbiome, and the extensive interaction between the microbiome and the human body from infancy to maturity as evidence that “in a very real sense, humans and their microbiome thus form a composite organism, a so-called holobiont.”61 Some specialists, such as Bordenstein and Theis, distinguish a holobiont from a superorganism by describing the latter as “an assembly of multiple individuals from the same species” and the former as “composed of multiple domains of life, as well as viruses.”62

From a technical standpoint, biologists and evolutionary theorists developed the holobiont evolutionary model in an effort to quantify how a symbiotic relationship between two or more organisms (“symbiogenesis and symbionticism”) leads to the development of new body shapes and functions (“morphologies and physiologies”).63 In this theory, “the ‘living together’ of ‘dissimilar’ …organisms” is one of the key mechanisms of speciation.64 The term holobiont is composed of holo meaning “whole” and biont meaning an “individual organism.”65 Thus, individual organisms (bionts) living mutualistically (where both sides benefit) in prolonged or permanent contact with one another comprise a holobiont. Evolutionary theorists and biologists are extending this theory, however, far beyond science “over into the arts.”66

Holobiont models of microbial/mammalian mutualistic evolution are being adapted to account for human self-consciousness and the ‘self.’67 For example, advocates of “Cognition Based Evolution” argue that, despite our subjective conscious experiences which tell us that we are “an organic singularity,” in reality the “accumulating evidence indicates that we are a multi-species collective.” In other words, human existence and consciousness are the products of a “holobionic partnership between our innate cells and an obligatory microbial fraction.”68 Human existence and our self-awareness of that reality, according to this model, arose (or arises) out of the interaction between human cells and the human microbiome: “our singular ‘self’ [is] an illusion.” Additionally, they claim that, because our existence today is the product of microbial/mammalian interaction in the past, our survival in the future as well as our evolution in the past is tied directly to the microbiome. What is at stake in this discussion is nothing less than what it means to be a human created in the image of God. If Darwinian evolution raised challenging questions about our ability to differentiate between animals and humans with regard to origins and anatomy, then holobiont models of microbiome/human co-evolution raise even more challenging questions about our ability to differentiate between humans and the human microbiome with regard to consciousness and ontology.69 Simply put, where do they end, and we do we begin?

At first glance, these definitions may seem like fanciful over-exaggerations; however, we must take these claims by microbiome researchers seriously. For, as Kunnen and Carlson note, without our “microbial partners we lack what we need to exist, let alone thrive.”70 Indeed, they rightly assert in their article that we ought not be surprised to discover that “we are completely interdependent on the smallest inhabitants of our world.”71 They further underscore the significance of the relationship between human “health and wellbeing” and “the health and wellbeing” of the human microbiome.72 However much we may desire to push back against the claims of microbiome research, its findings infringe on the question of human personhood. We cannot address its substantial anthropological and ontological claims without ignoring or minimizing the reality that “we are completely interdependent” on “the last and least within us.”73

Bonhoeffer’s Relational Image

Back when microbes were firmly viewed as invaders and merely the cause of diseases, Dietrich Bonhoeffer adapted a theme from Hegel in order to define human beings sociologically within the context of the church.74 Bonhoeffer’s model in Sanctorum Communio (1930) paints a picture of humans as fundamentally relational beings.75 In his dissertation, Bonhoeffer argues that at their most basic level humans exist communally in a state of “receptivity and reciprocity” with “others.”76 This community-oriented relationship is ethically dialectical: “I no longer control the other, nor does the other control me, but we both discover our individual and social identities in the place of our difference.” Humanity’s “source of self…resides…in the space of the relational between” and arises through the recognition of alterity or otherness.77 This relationally-oriented anthropology is carried forward and expanded in the work of other theologians such as Karl Barth, Jürgen Moltmann, Colin E. Gunton, and others, and can be adapted to incorporate the emerging data and claims of microbiome researchers.

Bonhoeffer’s model of the imago Dei—in addition to offering an inter-relational model of personhood—installs two guardrails or essential relationships to keep Christian theological models of personhood on an orthodox track. Additionally, it insists on one unwavering principle for any Christian model of personhood. First, Bonhoeffer points out that the concepts of community and personhood are “essentially related.”78 Since what it means to be a human person necessarily incorporates a definition of human community; to define one is to define it in relation to the other. While not identical, they do exist in a mutualistic relationship to one another. Any reconsideration of human personhood in light of the microbiome must define the human microbiome in relation to humanity in such a way that a distinction remains between individual life forms and the larger biological community. Every individual cannot become a community; however, individuals can no longer define themselves entirely in isolation. Part of Bonhoeffer’s reason for developing this inter-relational model was to address the individualism inherent to Hegel’s Idealism.

The second guardrail or essential relationship that Bonhoeffer identifies is that one’s definition of a human person carries implications for one’s “concept of God,” because human beings are created in God’s image.79 Quite simply, one’s conception of God and the image of God in humanity correspond to one another. This relationship can function as both a restraint and guide for new paradigms of theological anthropology. What are the implications for the imago Dei, as Kunnen and Carlson state in their article, given that “we are completely interdependent on the smallest inhabitants of our world?” We will return to this question below, as we consider Colin E. Gunton’s discussion of perichoresis.

After surveying four historical theories of the “basic-relations of social beings” in Sanctorum Communio, Bonhoeffer rejects Idealism and concludes that any sufficiently Christian theological anthropology must retain a “voluntaristic concept” of both God and humanity.80 Bonhoeffer’s concern in SC is to reject both the assertion of Idealism that creation is necessary for God and to affirm “the situation of responsibility” in which humanity is placed by God. As Steven Bouma-Prediger affirms in For the Beauty of the Earth (2010), what makes humans “unique” is that “we are God’s vice-regents”—human beings are morally responsible before God.81 This core component of the imago Dei thus necessitates some version of voluntarism. In light of the claims of microbiome research, voluntarism is a crucial concept which must be retained in any modern Christian attempt to account for human personhood and cognition. No matter the extent of the microbiome’s influence and/or impact on human personhood and cognition, we must not so elevate the second brain that the first brain becomes purely passive. We ought not elevate the “will” of the microbiome such that the human will becomes a mere puppet in the hands of microbial overlords.

An Analogy of Relation not Being

After considering the historical definitions of the imago Dei, Bonhoeffer chooses one which reflects an analogy of relation [analogia relationis] between God and man as opposed to an analogy of being [analogia entis]. As mentioned previously, the latter analogy revolves around fixed human attributes (mind, will, and/or affections) and is often associated with substantialist models of the imago Dei, in which some substance or quality within human beings ‘images’ God.82 J. Richard Middleton summarizes this paradigm—which he notes that “most patristic, medieval, and modern interpreters” have relied upon—as the ongoing attempt to answer the “speculative question: In what way are humans like God and unlike animals?”83 The classic example being, as David Cairns summarizes, that “up to Aquinas we find the image of God conceived in man’s power of reason.”84 This model, according to Middleton, led theologians such as Augustine to look for “intrapsychic trinitarian structures … which correspond to the triune nature of God” in the mind such as “memory, intellect, and will.”85 For a more in-depth discussion of the historical evolution of substantialist and relationalist models as well as the case for a functionalist model—which ties the imago Dei to humanity’s function as stewards in Gen. 1:28—see Middleton’s discussion in The Liberating Image: The Imago Dei in Genesis 1.

Other theologians, including Bonhoeffer, have recognized the individualistic drawbacks and dualistic assumptions inherent to an analogia entis between God and man. For example, in Colin E. Gunton’s estimation, substantialist definitions contributed to a Kantian epistemological framework which placed human reason and will at the center of human being, situating individuals at the center of their own reality: “I can will you as an end in yourself, or as a mere means to my end.”86 In an attempt to counter this model, Karl Barth pointed out that no one can exercise freedom in isolation, instead freedom is always exercised in relation to an Other: “As God is free for man, so man is free for man….”87 For Jürgen Moltmann, this relationality extends beyond the “possession of any particular characteristic” to humanity’s “whole existence,” which is “bound up with nature,” with God, and with other humans in the context of community. 88 Bonhoeffer too sought to overcome individualistic models of humanity by construing “the image of God… not as an individualistic attribute but as a particular social relationship between persons, based on the relationship of God to humanity.”89

Additionally, Bonhoeffer notes in Creation and Fall that substantialist models have historically relied upon a dualism between the spirit [Geist] or soul of human beings which images God, and the body [Natur] which does not or which is merely instrumental in carrying out the role of image-bearer.90 He rejects this view which bifurcates humanity, trapping our true selves in the prison of a body. The imago Dei is not foreign to the earth and the material.

It is my world, my earth, over which I rule. I am not free from it in the sense that my essential being, my spirit [Geist], has no need of a nature [Natur] which is alien to my spirit. On the contrary, in my whole being…I belong wholly to this world; it bears me, nurtures me, holds me….What so peculiarly binds human beings…is the authority conferred on humankind by nothing else than God’s word.91

Humanity’s function as image-bearers and stewards is therefore tied to relationality itself and is ontologically rooted “precisely in…bodily nature. For in [our] bodily nature [we] are related to the earth and other bodies.” 92 We are similarly related to the microbiome in our bodily nature.

Bonhoeffer and others thus redefine substantialist attributes such as the will or reason as things which humans possess but which are “not [possessed] …in a vacuum”—rather, they are possessed in relation to an Other. At the most fundamental level, human beings possess capacities such as freedom and reason in relation to the divine Other, God. Additionally, Bonhoeffer defined human freedom and its exercise in terms of “a relation between two persons”—a “being-free-for-the-other.”93 Thus, even those characteristics which individuals possess are not “individualistic…as a substance” in and of themselves.94 The imago Dei, according to this model, is not analogous to God in terms of individual attributes of being—“in which human beings, in their own existence in-and-of-themselves … could be said to be like God’s being”—rather, human beings have been “set” in relation to one another, to Creation, and ultimately to God in such a way that they are “free for one another” or free for the Other, as opposed to being “free from” others.95

As previously discussed, these fixed attributes of being are infringed upon by microbiome research. Defining what it means to be human using these characteristics alone is becoming increasingly problematic. Using Middleton’s “speculative question” as an example, it is increasingly difficult to answer how humans are “like God” by quantifying how humans are “unlike animals.” Bonhoeffer’s model, however, enables us to incorporate the human microbiome or gut microbiota as a player or contributor to the human central nervous system in a way that does not infringe upon or diminish the imago Dei but instead deeply reflects the nature of our Triune Creator. For this reason, Bonhoeffer’s sociological model is even more relevant today than it was almost 100 years ago. How then can his definition of the imago Dei be reformulated to account for the human microbiome?

In Relation to the Other

We can adapt from Sanctorum Communio, Bonhoeffer’s argument that human persons become ‘human’ when viewed or placed in relation to an Other, as a way of accounting for the aforementioned holobiont ‘self.’96 Bonhoeffer claims that only when the “concrete ethical barrier of the other person is acknowledged” can humans “grasp the social [ontological]-ethical basic-relations of persons.”97 In other words, only when other humans are recognized as an “ethical barrier” one ought not cross, only then, can an individual grasp what it means to be human. Other humans are a ‘You’ for us (a concrete ethical barrier) because of God’s gift of being: “the divine You created the human You….[Thus,] the other person is only a You insofar as God brings it about.”98 We can affirm this to be true with regard to the human microbiome as well. Humans were not colonized by invaders, nor did we arise out of an atheistic holobiont symbiogenesis; rather, God created humanity—along with the rest of creation—together with a microbiome. God freely decided to bring it about that our microbiome functions as a ‘Them’ or impersonal ‘You’ within our own bodies. Stated more personally, there is a community living within me and this community represents a kind of Other over which I do not have absolute control. Recognizing that the actions I undertake impact my microbiome and that those actions in turn impact me, in a feedback loop of causation, enables me to better grasp what it means to be a steward-priest over Creation, created in the image of God.

The Creator made not only other humans but Creation itself as a limit, an ethical barrier. Bouma-Prediger exhorts us to acknowledge that “creational finitude” should generate certain “ethical principle[s].”99 Living on a finite planet with finite resources is an ethical limit. The microbiome represents yet another ethical limit, except that it is part of us in a way that the external creation is not.

Once again, there is no need to embrace either a purely atheistic model of holobiont evolution in which human self-awareness and consciousness arise out of interactions between microbes and mammals, nor one in which human self-awareness and consciousness arise in our isolated minds because of some innate capacity—as in a vacuum. For, if human beings are created to be ethically accountable before God, we should expect that our self-awareness, ethical accountability, and consciousness would arise out of our “ethical-social interactions” with God and other humans.100 Even Adam stood before his Creator among a garden of creatures. In other words, because “God, community and individual[s]” are interconnected by God’s design, every human ‘I’ necessitates a ‘You.’101 This ‘I-You’ relation conceives of persons as poles within a multi-polar community of God and others. Clifford J. Green describes this model as “inter-personal personalism,” where instead of our basic relation being “cogito ergo sum” it is “I relate ethically to others, ergo sum.”102 As it relates to holobiont models and the claims of microbiome research, we can thus embrace the human microbiome as an ethical barrier or limit built into human beings by God. Since part, if not most, of what it means to be created in the image of God entails ethical responsibility—toward others, human community, and creation—“human beings do not exist ‘immediately’ through themselves qua Geist”; rather, human beings exist always “in responsibility as we encounter an ‘other.’”103 The microbiome can thus function as a created other residing in and on our bodies.

Colin E. Gunton’s discussion of the perichoresis of time, space, and relationality in The One, the Three and the Many (1993) offers another affirmation of this updated mammalian/microbiome model. If, as Gunton writes, “God is what he is by virtue of the dynamic relatedness of Father, Son and Spirit,” it is fitting to discover that we are what we are by virtue of the dynamic relatedness of our human bodies, the microbiome, and other human beings.104 That the human microbiome contributes to our “being” in some way, and that microbes in general contribute “to the being of everything else” is entirely consistent with a universe designed by a triune Being. Indeed, the implication of microbiome research is that even on the smallest biological level, as Gunton declares concerning all Creation, “reality is… perichoretic, a dynamism of relatedness.” Therefore, there is no theological reason to fear the possibility that the gut microbiota overlaps, interpenetrates, and/or participates with human freedom, reason, or physiology. And yet, Gunton beckons us further, noting that the import of “perichoretic being”—as the definition of what it means to be “created in the image of God”—is a “notion that has rarely been taken seriously.”105 He challenges us to extend this trinitarian conception beyond relationships between organisms: “it is not simply that we enter into relationship[s] with” other human beings; rather, “persons mutually constitute each other, make each other what they are.”106 The idea that gut microbiota play a crucial role in human physiology in no way seems foreign to the concept of perichoretic being. It may in fact be the case that we are not merely related to the human microbiome; rather, on some level, it constitutes part of us or makes us who we are. This conclusion is not hostile to a thoroughly trinitarian theology.

Considering Claims and the Use of Caution

In their 2017 article on the human microbiome, “Deeply Connected to God’s Good World,” Kunnen and Carlson advocate for the “use [of] humility as we consider the claims from microbiome research.”107 They point to two key factors which ought to give Christians restraint. First, they state that “all…corners of creation” are “fallen.” Therefore, the “very science [of the microbiome] is fallen, too.” Secondly, they highlight “substantial gaps in our understanding of which microbes” impact human health. Because of this, they claim that, “wrong experiments are done, coming to the wrong conclusions.” Thus, while they affirm that “we should expect to continue to find that these relationships are critical to who we are”; ultimately, they caution us to “wait for science to progress.” While these two assessments are technically accurate, I fear that they may function as excuses to ignore or diminish the claims of microbiome research.

First, while there are gaps in microbiome research and there is a need to qualify and clarify its claims, there are many reasons to take these claims seriously. Critics commonly point to the fact that most of the studies performed in this field rely on animal subjects—particularly gnotobiotic (bacteria-free) mice—and not humans. Indeed, with the exception of Tillisch et. al. (2013) and Messaoudi et. al. (2011), most studies cited in this paper predominantly rely on animal data. Despite these mitigating factors, critics should acknowledge that similar mice and animal models have been critical to the development of many modern drugs and medical treatments. Indeed, in their 2018 review of the types of mice and experiments used in testing the neurological effects of the microbiome, Zara et. al. acknowledge that “animal models are essential for the study of human disease and for the development of better treatments.”108 Not only are mice used to test drugs—some of which move on to human trials and are used in human bodies as legitimate medical treatments—several of the same types of mice and experiments used to test the psychobiotic and neurological effects of gut microbiota have also been used to measure the effects of Prozac and other neurological drugs.109 Indeed, microbiome research will continue to rely on mice because many crucial procedures would be not only impossible but ethically-objectionable to perform on humans. For example, one procedure used to verify a key pathway of the gut-brain axis is a “vagotomy”—the surgical severance of the vagus nerve.110 In light of these ethical challenges and in light of differences between mice and animal physiology, scientists will likely continue to struggle to draw clear distinctions between correlation and causation. We can assume that these challenges and gaps between observation and proof will persist. Many gaps may never close. I do not believe, though, that we should “wait for science to progress” before beginning to wrestle with the claims of microbiome research.

Secondly, while Kunnen and Carlson are right that science—like all methods of knowing—is “fallen,” this is an unclear and subjective precedent for evaluating and/or rejecting the conclusions of microbiome researchers. Labeling microbiome “science [as] fallen,” however scripturally accurate, rather than helping adjudicate between the claims of science and theology, may too easily function as the rationale for writing off or ignoring the claims of microbiome science that we dislike. Christians, unfortunately, have a track record of using this rationale to dismiss the claims of science. For that reason, both science and theology should engage in a dialogue among professionals in order to assess, independently verify, and incorporate various claims within their respective fields of study.

Biologists and biology students are asking themselves now, in light of the claims of microbiome research, “well, who am I then?” Christians of all stripes should be discussing the profound implications which follow from these claims. There is a deep need for theologians to use their knowledge and experience to engage with and address head-on these claims and their attendant anthropological models.

Aside: Redeeming the Microbiome

Questions naturally arise as to whether Jesus had a microbiome. Space does not permit a full discussion of this question, but how you answer it will likely be determined by your answer to two related questions. First, to what extent do you think Jesus will or is “making all things new” (Rev. 21:5)? Secondly, to what extent do you consider the microbiome integral to the definition of a human being? Your responses to these questions will significantly impact whether you want to affirm that Jesus had a microbiome and that it was ‘redeemed.’ Once again, while space does not permit a proper exegesis, there seem to be biblical examples that point to the existence of ‘redeemed microbes’ in passages such as Isaiah 25:6-9, Luke 22:18, and Revelation 19:6-9. They paint a picture of the Bride of Christ drinking wine and eating food at the Marriage Supper of the Lamb. Why would eschatological wine not be fermented by ‘redeemed’ microbes and eschatological food not digested by a ‘redeemed’ gut microbiota? I am indebted to Dr. Crystal Downing, Co-Director of the Marion E. Wade Center, for the observation that in order for many Christians to celebrate the Eucharist now, they depend on the work and participation of microbes for both the elements: leavened bread and fermented wine. To partake of Christ’s body requires the work of not only the Holy Spirit but of the Spirit’s work through yeast in the bread and bacteria in the wine. The mind reels with questions about this topic. Personally, I would affirm that the human microbiome, in its own way, “groan[s] within ourselves, eagerly awaiting…the redemption of our bodies” (Rm. 8:23).


The relational model of the imago Dei presented in this article can account for both the current and future claims of microbiome research. Ontologically, it enables us to embrace the idea that individuals cannot live flourishing lives without their gut microbiota. For, regardless of the extent of the microbiome’s participation in or influence on human freedom, reason, and physiological uniqueness, we can affirm that removing your gut microbiota would somehow make you less ‘you.’ Ethically-socially, no matter the extent of the interaction between an individual’s gut microbiota and their first brain, we can embrace the microbiome as a yet-to-be-fully-quantified ethical barrier within every human person. To adapt Bonhoeffer’s ‘I-You-relation’ language, we can view the human microbiome as a “limit for the subject” and can even affirm the possibility that the gut microbiota’s “own will activates a will that impinges upon the other” such that the microbiome “become a You for the I.”111 Practically, to transgress one’s gut microbiota (to fail to care for this ‘other’ within) leads to real consequences ranging from dysbiosis, disease-processes,112 and ultimately the inability to live out the second commandment.

In her paper, “Loving Our Neighbors: Responsibility in the Created World,” Dr. Kirsten Page, Ruth Kraft Strohschein Distinguished Chair & Professor of Biology at Wheaton College, argues that all creation care or environmentalism is a form or a way of loving one’s neighbor.113 She contends that while “our patterns of consumption” are not our neighbor, they have concretely contributed “to the current ecological crisis” facing our world. They impact our neighbor.114 How we treat our immediate environment either directly or indirectly leads to the flourishing or harm of our neighbor; therefore, “[care] for creation is love for our neighbors.”115 Surely, this applies to the most immediate environment of the microbiome in and on our bodies?

Therefore, how we care for our microbiome impacts our ability to love our neighbor, to live out the second greatest commandment (Matt. 22:38); because, at a most basic level our gut microbiota impacts our ability to live a flourishing life and to minister to others. In her article, Page laments the fact that Christians have traditionally “been slow” to develop a “Christian response” to problems of “environmental degradation and the suffering of the poor from disease.”116 To call the Christian response to such environmental crises slow is kind. Talk of environmentalism or even “creation care” is often written off as scare-mongering, quack science, evidence of a fallen world, or as not trusting in God’s sovereignty over the earth. It is easy to dismiss the fate of animals and trees because we do not value them as we value humans. As Bouma-Prediger decries, we too easily give instrumental not intrinsic value to non-human aspects of creation.117 We assume that they are here for us, not we for them.

The microbiome represents a new ecological problem. Its degradation—through the ubiquity of processed food, the overuse of antibiotics, increasing industrialization, and a century of microbial warfare waged by twentieth-century medicine—has resulted in a new type of ecological crisis which is directly impacting human health. Scientists like Rodney Dietert are sounding alarm bells about the ecosystem within the human gut and its potential connection to the increase of non-communicable diseases [NCDs] in Western nations, which is placing an unbearable strain on the finances of modern healthcare systems. On a daily basis, NCDs correlated with dysbiosis of the gut microbiota are hampering the ability of Christians to love their neighbors and preventing them from living out the second greatest commandment. The clearest example of this can be seen in the obesity epidemic facing modern America.

What Page states about the broader environment is true of the microbiome environment within: The neglect of “our relationship with non-human creation” is a failure “to be appropriate caretakers.” Knowing that “we are called by God to be stewards of His creation” means that our “failure to respond is direct disobedience, and therefore sin.”118 To what extent are we willing to acknowledge our dependence on the microbiome, to view it as an ethical limit and obligation, alongside our broader calling as image-bearers?

The discovery of the microbiome’s impact on human physiology is challenging long-held substantialist models of the imago Dei, yet it is revealing what we should have suspected all along, that there is a mind-boggling level of perichoretic relationality built into not just creation but every human being. Ed Yong writes in I Contain Multitudes (2016) that “there are more bacteria in your gut than… stars in our galaxy.”119 Our increasing knowledge of these “multitudes within” and their relationship to human flourishing ought to fundamentally alter the way we define not only what it means to be human, but also our responsibility to God’s creation. By defining the image of God in terms of our relationality to God, to each other, and to creation—especially the microbiome within—we can celebrate, alongside Bonhoeffer, that “God, the brother and sister, and the earth belong together.”120 We can declare, along with Joseph Sittler, that, “creation is a community of abounding life—from the invisible microbes to the highly visible elephants….These companions…are not only there: they are there as things without which I cannot be at all! They surround, support, nourish,…challenge, and talk back to us.”121

Cite this article
Aaron M. Hill, “The Other Within: Rethinking Theological Anthropology in Light of the Microbiome”, Christian Scholar’s Review, 50:1 , 39-59


  1. William Beaumont, Experiments and Observations on The Gastric Juice, and the Physiology of Digestion (Boston: Lilly, Wait, and Company, 1834), 8.
  2. Ibid., 9.
  3. Ibid.
  4. Ibid., 11.
  5. Ibid., 78, 98.
  6. Robert G. W. Kirk, “Life in a Germ-Free World: Isolating Life from the Laboratory Animal to the Bubble Boy,” Bull Hist Med 86.2 (2012): 237–275; Rodney Dietert, The Human Superorganism: How the Microbiome is Revolutionizing the Pursuit of a Healthy Life (New York: Penguin Random House, 2016), 5.
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  11. Ibid., 3.
  12. In addition to other theologians like John Zizioulas, Colin Gunton, and Joseph Sittler.
  13. Steven Bouma-Prediger, For the Beauty of the Earth: A Christian Vision for Creation Care (Ada, MI: Baker Academic, 2010), 115.
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  37. Ibid., 135-36.
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  50. Timothy G. Dinan and John F. Cryan, “The Microbiome-Gut-Brain Axis in Health and Disease,” Gastroenterol. Clin. N. Am. 46 (2017): 84.
  51. Cryan and Dinan, 704.
  52. For example, studies 48-59 in Cryan and Dinan, “Mind Altering Microorganisms,” 705-706.
  53. For example, O’Mahony et. al. (2015) summarizes the behavioral impact of “the gut microbiota, tryptophan metabolism and the serotonergic system” on germ-free mice. They cite studies that point to changes in “anxiety-like behaviours,” “depressive-like behaviours,” and “cognitive function.” See also Ridaura, et al. “Cultured Gut Microbiota from Twins Discordant for Obesity Modulate Adiposity and Metabolic Phenotypes in Mice,” Science 341.6150 (2013); Ellekilde, et al. “Transfer of Gut Microbiota from Lean and Obese Mice to Antibiotic-treated Mice,” Sci. Rep. 4 (2014).
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  56. Rees et. al., 4.
  57. Dietert, 38-39; “The coral reef was the original source for the term ‘holobiont,’ coined in 1992 by theoretical biologist David Mindell.”
  58. Ibid., 26.
  59. Kunnen and Carlson, “Deeply Connected to God’s Good World,” CSR 46.2 (2017): 120.
  60. Dieter, 26; See also Seth R. Bordenstein and Kevin R. Theis, “Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes,” PLOS Biology 13.8 (2015): e1002226; Angela E. Douglas and John H. Werren, “Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts,” mBio. 7.2 (2016): e02099-15.
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  62. Bordenstein and Theis, 8.
  63. Ibid.
  64. Lynn Margulis, ed., Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis (Cambridge, MA: MIT Press, 1991), 1.
  65. Ibid., 2.
  66. Rees et. al., 4.
  67. William B. Miller Jr., John S. Torday, František Baluška, “Biological Evolution as Defense of ‘Self,’” Progress in Biophysics and Molecular Biology, in press, corrected proof (October 16, 2018): 1.
  68. Ibid.
  69. Ibid., 2.
  70. Dietert, 68.
  71. Kunnen and Carlson, 124.
  72. Ibid.
  73. Kunnen and Carlson, 124.
  74. Charles Marsh, Reclaiming Dietrich Bonhoeffer: The Promise of His Theology (New York: Oxford UP, 1994), 88-89.
  75. Clifford J. Green, “Editor’s Introduction,” in Sanctorum Communio: Dietrich Bonhoeffer Works, Vol. 1. [SC] (Minneapolis, MN: Fortress Press, 1998), 4.
  76. Dietrich Bonhoeffer, Sanctorum Communio: Dietrich Bonhoeffer Works, Vol. 1. [SC] (Minneapolis, MN: Fortress Press, 1998), 69.
  77. Ibid.
  78. Ibid., 34.
  79. Ibid.
  80. Ibid., 48-52.
  81. Bouma-Prediger, 115.
  82. Dietrich Bonhoeffer, Creation and Fall: Dietrich Bonhoeffer Works, Vol. 3 [CF] (Minneapolis: Fortress Press, 1997), 11; Colin E. Gunton, The One, the Three and the Many (Cambridge University Press, 1993), 52-58; For an extended historical discussion of these three views of the imago Dei see J. Richard Middleton, The Liberating Image: The Imago Dei in Genesis 1 (Grand Rapids: BrazosPress, 2005), 15-41.
  83. Middleton, 18.
  84. Qtd. in Middleton, 18; David Cairns, Image of God in Man. The Fontana Library of Theology and Philosophy (London: Collins, 1973), 116.
  85. Middleton, 18.
  86. Gunton, 53.
  87. Barth, Church Dogmatics, Creation, III.1, §40-42: The Doctrine of Creation, Study Edition 13 (London: T&T Clark, 2010), §41.2, 193.
  88. Jürgen Moltmann, God in Creation: A New Theology of Creation and the Spirit of God. trans. Margaret Kohl (Minneapolis: Fortress Press, 1993), 221.
  89. Clifford J. Green, Bonhoeffer: A Theology of Sociality 1972, rev ed (Grand Rapids, MI: William B. Eerdmans, 1999), 190.
  90. CF, 66.
  91. Ibid.
  92. Ibid., 79.
  93. CF, 63.
  94. Ibid.
  95. Ibid., 65-66.
  96. SC, 50-52.
  97. Ibid., 50.
  98. SC, 54f; Green, 35.
  99. Bouma-Prediger, 139.
  100. SC, 50.
  101. Ibid., 51.
  102. Green, 30.
  103. Ibid., 31.
  104. Gunton, 165-66.
  105. Ibid., 168-69.
  106. Gunton, 169; Gunton is quoting from John MacMurray, Persons in Relation (London: Faber, 1961), 17, 69.
  107. Kunnen and Carlson, 124.
  108. N. Z. Kara, M. Y. Stukalin, and H. Einat, “Revisiting the Validity of the Mouse Forced Swim Test: Systematic Review and Meta-analysis of the Effects of Prototypic Antidepressants,” Neuroscience and Biobehavioral Reviews 84 (2018): 1.
  109. John F. Cryan, Athina Markou, and Irwin Lucki, “Assessing Antidepressant Activity in Rodents: Recent Developments and Future Needs,” TRENDS in Pharmacological Sciences 23.5 (2002): 243.
  110. El Aidy et. al., “Microbiome to Brain,” 319.
  111. SC, 51.
  112. See Dietert, “Patterns of Disease” in The Human Superorganism, 123-140.
  113. Kristen Page, “Loving Our Neighbors: Responsibility in the Created World,” CACE eJournal (2006): 1-52.
  114. Ibid., 33.
  115. Ibid., 31.
  116. Ibid., 32.
  117. Bouma-Prediger, 165.
  118. Page, 32.
  119. Ed Yong, I Contain Multitudes: The Microbes Within Us and a Grander View of Life (New York: Ecco, 2016), 8.
  120. CF, 67.
  121. Joseph Sittler, Evocations of Grace: The Writings of Joseph Sittler on Ecology, Theology, and Ethics (Grand Rapids, MI: William B. Eerdmans, 2000), 204.

Aaron M. Hill

Southwestern Baptist Theological Seminary
Rev. Aaron M. Hill is the Production Editor for VII: The Journal of the Marion E. Wade Center and holds an M.A. in Systematic Theology (2019) from Wheaton College in Wheaton, Illinois and an M.A. in Christian Education (2007) from Southwestern Baptist Theology Seminary in Fort Worth, Texas.