Beyond the Organism
We have the late American evolutionary thinker Lynn Margulis (1938-2011) to thank for the rising profile of the concept of the holobiont. Margulis was the preeminent champion of the vital evolutionary role played by symbioses—those biological and ecological relationships by which two or more different organisms make their living in continuous bodily contact with each other. The holobiont concept views living systems as constituted by their embeddedness in the matrix of their symbioses. This concept goes beyond the traditional definition of an organism as a biological individual to include the full roster of other life-forms— including bacterial, protistan, or fungal partners—that dwell in stable contiguity with each other and functionally combine to make and maintain that larger consortium. She did not coin the technical term holobiont, but her writings in the 1980s and ’90s effectively brought it into wide use.
In the second edition of her major scientific work Symbiosis in Cell Evolution, Margulis illustrates the holobiont concept in relation to the life cycle of the lichen, a symbiotic organism arising from the cross-kingdom integration of a fungus with a bacterium or a protist such as an alga. In this particular example of a mutualistic symbiosis, as Derek Woods aptly puts it, “The fungus is a greenhouse for the alga and the alga is a solar panel for the fungus.” When integrated into a lichen, the fungus and the alga retain their genetic and autopoietic identities even while expressing tissues that are unique to their direct contact within the emergent holobiont.
The lichen is both a special and a paradigmatic case. In the plant and animal kingdoms, holobionts are typically analyzed into their macroscopic hosts and their microbial symbionts. The feminist theorist Donna Haraway insists, however, that the host is as much a symbiont of its microbes as they are of it. And since it is symbioses all the way up and down, the holobiont transcends the traditional concept of biological “individuals,” since strictly speaking, a holobiont is a community of organisms, an entire integrated ecology, a system of nested beings.
You, too, dear reader, are a holobiont. Your healthy early development as well as your daily well-being depend on a thriving microbiome that makes its living inside your tissues. Your formation as a holobiont began when you descended your mother’s birth canal and picked up her maternal microbial complement, a starter kit for your own nascent microbiome. In this way, you inherited your first symbionts from your mother—not genetically, but rather, environmentally, or epigenetically. As a holobiont host, your symbiotic complement is then continuously refreshed throughout your life cycle through your various interactions—breathing, eating, clambering about—with your world, and especially, with other holobionts.
Only in the last few decades has the concept of the holobiont gained prominence as an authoritative scientific description of the actual ecological complexity of no-longer “separate” organisms. The vital symbiotic dynamics brought into sharp focus by the holobiont concept were previously pushed to the margins of biology, for one reason, because they did not have strictly to do with traditional Darwinian matters such as the survival of the fittest through reproductive fitness. Such descriptions relied precisely on the notion of genetic individuality and the selection of its supposedly random variations. However, by now the holobiont concept has generated a vigorous scientific literature dedicated to overcoming the individualist ideology that saturated earlier biological concepts. For instance, it is currently being debated to what extent Gaia itself—the planetary system integrating life altogether with its geological environment—may be considered as a planetary holobiont.
The Planetary Holobiont
Lynn Margulis’s recovery of the pervasive significance of symbiosis, her resurrection and reestablishment of that concept as a fundamental biological and ecological dynamic, developed concurrently with her participation with James Lovelock on the elaboration of the Gaia concept. For Margulis, Gaia may be considered as the sum of all symbioses. And if we value life equally in its willingness to come together, its propensities for collectivity, then Haraway’s recovery of the concept of sympoiesis—the generative association of living entities with other life-forms of the same and different kinds—may now also inform the notion of Gaia as the planetary iteration of the holobiont.
In “Beyond the Organism” we started with the lichen as holobiont and then moved to humans as holobionts. Now we come to the planetary scale of considering the Gaian system as the final iteration or ecological summation of the holobiont dynamic. Framing Gaia as the planetary holobiont is in fact an improvement on earlier speculations considering Gaia as a planetary organism, a notion that still retained the holistic implication of individuality or singularity. Mortality remains the case for every component of a terrestrial holobiont: each has to reproduce on its own in order to maintain the generation of its specific line. But Gaia does not really reproduce to give birth to another Gaia. It just persists and evolves, incorporating ever renewed components of ever-renewed ecosystems. Understanding Gaia as a planetary holobiont rather than as a planetary organism allows for this refined recognition of the multiplicity and differentiation that is also part of life writ large. Such lines of systemic closure and variation run alongside the sympoietic and aggregative tendencies of living systems as they bond with each other as well as with the Earthly critical zones that absorb and sustain their metabolic uptakes and outflows.
Biological evolution is thus an elemental phenomenon within the evolution of Gaia at large. As the microcosm evolves, as species evolve, Gaia evolves—there is a massive planetary feedback loop here operating over evolutionary time. And all the while, there is innovation, inevitable change. This is basic systems theory: despite a common mischaracterization, autopoietic systems cannot merely replicate themselves in perpetuity. This is because they are foundationally embedded in the changes they make to their own biotic and material environments, which then feed back incrementally upon the system. And if we are inside Gaia, then there is a sense in which Gaia is also inside us.
In this way, the holobiont and its microbiome also illuminate the more recent immunological thinking. In this reconception, the immune systems distributed throughout the biota not only marshal a militia of antibodies to combat invaders from the outside world. Equally consequentially, immune systems recruit microbes from the environment for the holobiont’s microbiome and operate on its behalf to preserve a healthy internal ecology. The symbiotic operations of immune systems on behalf of their holobionts are a microcosm of what Gaia does for life on the planet. There is a comparable scene of mutualistic collectivity in the service of habitable conditions. This distribution of benefits ranges from the Gaian level of the biosphere to the discrete viability of the multispecies consortia gathered into every holobiont’s meta-organismal collective and back again.
