By Nick Anderman, December 2016
UC Berkeley, Department of Geography
Over the past 15 years the study of tiny things has undergone a sea change. The development of new, high-throughput gene-sequencing methods has allowed microbiologists and scientists working in related fields to observe, analyze, and manipulate microbes at previously unimaginable volumes and resolutions. The result has been a reconsideration of fundamental theories of life on earth, with provocative implications for thinking about the relationships between humans and non-humans, nature and society (Lorimer 2016, Paxson 2008; Helmreich 2009, 2016). To date geographers have ignored this shift, despite pressing reasons to engage theoretically and empirically with what Dorion Sagan has called the new “facts of life” (2011). In this short essay I make the case for thinking geographically about microbes and, more specifically, microbiomes, i.e. diverse assemblages of microbes in a given environment. I begin with an overview of recent developments in microbiome research, paying particular attention to how the emergence of the microbiome as a unified object of study has given rise to a crisis of theory in microbiology. After issuing a call for new research into what might be called the geography of microbes, I briefly describe how thinking with a particular microbiome – that of the human gut – might generate novel approaches to ongoing debates about the concept of scale.
Microbes – including bacteria, fungi, nematodes, protists and other biological phenomena too small to be seen with the naked eye – are the “most numerous, diverse and ancient of the many life forms on our planet” (Duncan et al. 2013: 1), yet we know very little about them. Recent estimates suggest that earth is home to 1 trillion microbial species, of which we have identified around 0.01% (Locey and Lennon 2016). Perhaps most surprisingly, non-human microorganisms account for roughly half the cells that occupy the space we call the human body (Sender et al. 2016). These microscopic entities have causal effects on most aspects of our lives, including how we look and smell and see, how we think and feel, and to whom we are attracted. Furthermore, they have been shown to influence key biological and chemical life processes, including digestion, immunity, cognition, reproduction and evolution. In short, life – and particularly human life – is today increasingly understood to be multiple, emergent and processual – an “open thermodynamic system, as well as an open informational one” (Sagan 2011).
Evidence for these new conceptions of life has accumulated briskly over the past 15 years, primarily as a result of research on the human gut microbiome. The term microbiome came into widespread usage in microbiology in the early 2000s, when it was defined by the molecular biologist Joshua Lederberg as an “ecological community of commensal, symbiotic, and pathogenic microorganisms that literally share our body space and have been all but ignored as determinants of health and disease” (Lederberg & McCray 2001: 2). While traditional microbiology analyzed individual microbial species cultivated in laboratory settings, microbiome research aims to understand collections “of genomes derived from microbial communities sampled from natural environments”. The objective is to uncover not just the general characteristics of isolated microbes, but the lived “complexity of human microbial communities” (Human Microbiome Project DACC).
Rapid growth in biomedical microbiome scholarship since 2000 has yielded a huge amount of metagenomic data, led to the establishment of new academic positions and journals, and generated a rising tide of interest in the microbiome among social scientists, artists and the general public (Mendes-Soares et al. 2016). Nonetheless, as biologist Rob Dunn recently noted, when it comes to understanding our planet’s microbiomes “we live in a vast bed of ignorance” (2016). In part the confusion is attributable to the technical limitations of DNA sequencing tools; arbitrary but deeply inscribed disciplinary divisions within microbiology; and the sheer quantity of microbial life to be examined. To date microbiome researchers have focused almost exclusively on cataloguing the inhabitants of (mostly human) microbial communities, rather than “elucidating the principles that govern their assembly, dynamics and functions” (Waldor et al. 2015: 1).
More fundamentally, microbiome scholarship has generated pressing questions about the spatial and ontological status of microbial life. Traditional biogeographical theory holds that with regard to microbes “everything is everywhere and the environment selects”, meaning (1) microbes have such enormous dispersal power that they “rapidly erase the effects of past evolutionary and ecological events”; and (2) that “different contemporary environments maintain distinctive microbial assemblages” (Martiny et al. 2006: 103). The latter point indicates environmental determinism. However, as noted by a chorus of philosophers and anthropologists of biology, this hypothesis has been repeatedly undermined by recent research. Contemporary findings show differentiated microbial distribution patterns both within the bounds of individual microbiomes and at a range of spatial and temporal scales. Furthermore, new data suggest that microbial life is far more abundant, diverse and mutable than previously assumed. Microbes routinely mutate, recombine and are transmitted among various taxa and populations both within the human body and across an array of other environments. As a recent survey article in Trends in Microbiology put it, “microbial taxonomy and phylogeny are in perpetual flux” (Beiko 2015: 671).
Consequently, many of the key questions posed by microbiome research exceed the disciplinary bounds of traditional biological theory. For instance, is the human gut microbiome best understood as an organ unto itself, a community of human and non-human microbes, or an internal feature of our developmental environment? Should it be “assimilated into an overall ecological reconception of the human being as superorganism” (Huss 2014: 392)? Given the diversity and varied provenance of microbes in a given microbiome, where do we map its borders, and why? How do microbiomes and other groupings of microbes change – or, for that matter, maintain stability – over time? Do microbes/microbiomes have agency?
These questions intersect neatly with a slew of long-running debates in geography, including discussions about complexity, assemblage, materiality and morphology, to name only a few. Yet the microbiome has attracted scant attention from geographers (though see Lorimer 2016, Guthman & Mansfield 2013, Wynne 2005). Applying geographical concepts, methods and theories to microbial life is a necessary and worthwhile challenge, because taking the microbiome seriously – with all the methodological and conceptual hurdles this task implies – has potentially meaningful implications not only for microbiology but for geography as well.
In what follows I unpack a few of these implications with regard to the concept of scale. The term has generated much debate in geography in recent years. Broadly, scale is understood to have four major definitions (Marston et al. 2009: 664-666). First, in cartography it denotes map resolution. Second, it may be deployed as a methodological descriptor, naming the level (on a macro to micro spectrum) at which data are to be collected. A third approach takes scale to be a socially constructed ontological effect of powerful interests, particularly capital and the state. In this interpretation, benefits generally accrue to actors that operate – or can convincingly claim to operate – at the uppermost scale, traditionally one encompassing the entire world. Following on from this third meaning, the fourth (and newest) definition takes scale to be a highly politicized epistemology with no grounding in the material world. In its place, theorists have suggested a litany of non-hierarchical concepts, including assemblages, flat ontologies and various sorts of networks. The ongoing scale disputes in geography center primarily on the term’s third and fourth meanings, paying particular attention to their methodological and political implications.
How might thinking with microbes enrich this debate? An initial move in this direction might extend the “familiar cascade from micro (body) to macro (globe)” (Ibid 664) to include the body’s interior. But the process of extension cannot end there. For the human body “acts as an ecological landscape by harbouring many ecosystems and meta-communities, as well as biotic and abiotic determinants and barriers that prevent, and corridors that facilitate, dispersal” (Gonzalez et al. 2011: 779) of microbes. In terms of microbial distribution, then, the human body is a striated world unto itself. As such, one might posit a new scalar ladder within the confines of corporeal space, starting (for instance) with individual cells and moving up to unicellular microbes, complex microbes, simple microbial communities, complex microbial communities bounded within a single organ and onto multi-organ microbiomes of various morphological qualities. Presumably the largest scale in this corporeal scalar hierarchy would be the body in toto, thereby linking the micro-scalar hierarchy with the older macro order.
Taking up the third definition of scale summarized above, we might ask how these sub-dermal scales are (re)produced? This line of inquiry leads, first, to STS-inspired analyses focusing on the politics of the production of scientific knowledge. These could take any number of forms, including efforts to pry open the black box of DNA sequencing technologies, for instance, or inquiries into the basic taxonomical categories that underpin most contemporary research in microbiology. Other projects in this vein might investigate the role pharmaceutical companies have played in defining which micro-scales matter (and why) in a given microbiome, or how the state (in the guise of the National Institutes of Health or Centers for Disease Control and Prevention, for example) has directed microbiome research funding, and to what ends. This sort of research can contribute meaningfully to geographical understandings of scale.
Turning to the fourth and final definition of scale explicated above, I would like to suggest that the microbiome is a uniquely generative empirical example with which to interrogate the notion of ontological scale, for three reasons. First, it is difficult to say with any sort of precision where a particular microbiome begins and ends. Its boundaries are diffuse, arguably to the point of nonexistence. Take the human gut microbiome, for instance. Though nominally clustered within a specific space – the gastrointestinal tract – the community of microbes itself is remarkably extensive, both within the space of the body and outside it. Microbes, it seems, move (in large quantities) through us, around us and across vast distances (Brito & Alm 2016). Second, and relatedly, microbiomes tend toward extreme mutability, again nearly to the point of dissipation. The microbes that constitute the gut microbiome, for instance, are constantly in flux, as a result of a whole range of poorly understood processes, including the continual introduction of new microbes (primarily via the mouth but also from other parts of the body); the excretion of others; and frequent random mutations. Marston et al. claim that “scale is a classic case of form determining content” (2005: 422); conversely, the microbiome is a radical example of content determining form. Finally, third, I would like to suggest that the agential qualities of both microbes and microbiomes – their liveliness, broadly construed – incessantly undermines any understanding of them that is a priori scaled (see, for instance, Beil 2016). Various efforts to add complexity to the operational aspects of hierarchical scale with reference to bending and jumping cannot fully account for this vitality. This last point is admittedly a shaky proposition – I am not entirely convinced of it myself. All three points laid out here require further research, which is unfortunately beyond the scope of this paper.
 This is the so-called Baas-Becking hypothesis, first articulated in 1934 by the Dutch botanist and microbiologist Lourens Baas-Becking (O’Malley 2008).
Beiko, RG (2015) “Microbial malaise: how can we classify the microbiome?” Trends in Microbiology, 23(11): 671-679.
Beil, L. (2016) “Microbial matter comes out of the dark,” Science News: Magazine of the Society for Science & the Public, URL: https://www.sciencenews.org/article/microbial-matter-comes-out-dark, accessed: 5 December 2016.
Duncan, MJ and Bourrat, P, DeBerardinis, J, O’Malley, M. (2013) “Small things, big consequences: microbiological perspectives on biology,” The Philosophy of Biology, 2013, 1: 373-394.
Dunn, R. (2016) “The wild life of our bodies: geography, discoveries, new insights, and persistent ignorance,” Conference address. Gut Reactions: The Microbiome and Human Nature, Princeton University, March 30-31, 2016.
Gonzalez, A. and JC Clemente, A Shade, JL Metcalf, S Song, B Prithiviraj, R Knight. (2011) “Our microbial selves: what ecology can teach us,” EMBO Rep, 2011 Jul 1; 12(8): 775-84.
Guthman, J. and Mansfield, B. (2012) “The implications of environmental epigenetics: A new direction for geographic inquiry on health, space, and nature-society relations,” Progress in Human Geography, 37(4): 486-504.
Helmreich, S. (2009) Alien Ocean: Anthropological Voyages in Microbial Seas. Berkeley, CA: University of California Press.
Helmreich, S. (2016) Sounding the Limits of Life: Essays in the Anthropology of Biology and Beyond. Princeton, NJ: Princeton University Press.
Martiny, J.B.H., B. Bohannan, J. Brown, R. Colwell, J. Fuhrman, J. Green, M.C. Horner-Devine, M. Kane, J. Krumins, C. Kuske, P. Morin, S. Naeem, L. Ovreas, A.-L. Reysenbach, V. Smith, J. Staley. 2006. “Microbial biogeography: Putting microorganisms on the map.” Nature Reviews Microbiology 4: 102-112.
Human Microbiome Project DACC, About The HMP. Hmpdacc.org. N.p., 2016. Web. 3 Oct. 2016.
Huss, J. (2014) “Methodology and ontology in microbiome research,” Biological Theory, 9: 392-400.
Lederberg J. and McCray AT. (2001) ’Ome Sweet ’Omics—a genealogical treasury of words. Scientist, 15(7): 8.
Locey, KJ and Lennon, JT (2016) “Scaling laws predict global microbial diversity,” Proceedings of the National Academy of Sciences of the United States of America (PNAS), vol 113, no 21: 5970-5975.
Lorimer, J. (2016) “Gut Buddies: Multispecies Studies and the Microbiome,” Environmental Humanities, 8(1): 57-76.
Marston, S.A., J.P. Jones III and K. Woodward (2005) “Human geography without scale”, Transactions of the Institute of British Geographers, 30, 4, 416-432.
Marston, SA, K Woodward and JP Jones. (2009) The dictionary of human geography, 5th edition, edited by Derek Gregory, Ron Johnston, Geraldine Pratt, Michael J. Watts and Sarah Whatmore, “Scale, 664-666,” Malden, Oxford and Chichester: Wiley-Blackwell.
Mendes-Soares, H and Mundy, M, Soares, LM, Chia, N. (2016) “Mminte: an application for predicting metabolic interactions among the microbial species in a community,” BMC Bioinformatics, 17(1): 343.
O’Malley, M. (2008) “‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography,” Stud. Hist. Phil. Biol. & Biomed. Sci. 39 (2008): 314-325.
Paxson, H. (2008) “Post-Pasteurian cultures: The microbiopolitics of raw-milk cheese in the United States,” Cultural Anthropology 23(1): 15–47.
Sagan, D. (2011) “The human is more than human: Interspecies communities and the new “facts of life”.” Theorizing the Contemporary, Cultural Anthropology website. https://culanth.org/fieldsights/228-the-human-is-more-than-human-interspecies-communities-and-the-new-facts-of-life
Sender R and Fuchs S, Milo R. (2016) “Revised Estimates for the Number of Human and Bacteria Cells in the Body”, PLoS Biol 14(8): e1002533.
Waldor MK, Tyson G, Borenstein E, Ochman H, Moeller A, Finlay BB, Kong HH, Gordon JI, Nelson KE, Dabbagh K, Smith H. (2015) “Where next for microbiome research?” PLoS Biol 13(1): e1002050.
Wynne, B. (2005) “Reflexing complexity: Post-genomic knowledge and reductionist returns in public science,” Theory Culture and Society, 22: 67-94.