Individuality or the “holobiont” and its construction through the integration of microbes

Recent work on host-microbiotainteractions has led to the concept of the “holobiont”, to refer to a host and the symbiotic microorganisms that it harbors (Zilber-Rosenbergand Rosenberg 2008; Gilbert, Sapp and Tauber 2012). Though research conducted in the past ten years has undeniably used novel techniques (in particular in metagenomics: Turnbaugh and Gordon 2008) and produced new, often unexpected insights (Turnbaugh et al. 2007; McFall-Ngai et al. 2013), there is a long tradition of scientific, historical and philosophical work on symbiosis (e.g., Sapp 1994; Margulis 1998; Dupré and O’Malley 2009; Bouchard 2013).

A historical investigation will help clarify key conceptual debates, including one that generates many disagreements in present discussions and which concerns nothing less than the definition of the notion of “symbiosis” itself: according to some (e.g., McFall-Ngai 2002; Bouchard 2013), any long-lasting interaction between two biological entities belonging to different species should be called “symbiosis”, while for others (e.g., Hooper and Gordon 2001) the word “symbiosis” should be applied more narrowly to cases in which the interaction is beneficial to one partner and neutral to the other (“commensalism”) and cases in which the interaction is beneficial to both partners (“mutualism”).

This IDEM sub-project therefore aims at shedding light on present discussion over symbiosis, mutualism, “microbiota”and the “holobiont” thanks to a precise reconstruction of the conceptual and experimental steps that have led to the present vocabulary. As IDEM is interested in the construction of the organism through its dialogue with the microbiota, a fundamental challenge is to offer a detailed account of the way the organism acquires its symbionts throughout its life, from the very first step of its building to its death, and how it interacts with them in health and disease.

Gérard Eberl’s team has suggested that in mammals gut microbiota can induce the organogenesis of novel gut organs, called “isolated lymphoid follicles” (ILFs) (Eberl 2005). Such a claim is thought-provoking, in particular because it echoes work done on symbiont-dependent organogenesis in other model systems (McFall-Ngai and Ruby1991), but calling the induction of ILFs “organogenesis” might seem inappropriate to some, and discussions of this kind can be settled only with the help of conceptual analysis.

Another important question is to determine to what extent the microbiota itself “develops”: if the concept of “co-development” (Gilbert and Epel 2009) is taken seriously, then it follows that both the host and the microbiota “develop”, and do so thanks to their relationship. It is thus essential to understand in what sense the concept of “development” can be applied to the microbiota, a question that echoes the more general problem of determining whether microbes can be said to “develop” (Love and Travisano 2013).

Finally, the “holobiont” is often described as a unit of development (Hooper and Gordon 2001; Bosch and McFall-Ngai 2011) and sometimes as a unit of evolution as well (Zilber-Rosenberg and Rosenberg 2008), but, to our knowledge, no precise analysis of the kind of “unity” found in a holobiont has been provided until now. Is the holobiont really a physiological and developmental unit, and if so should it be understood as a legitimate biological individual? Or should it rather be conceived as a community, or an ecosystem (Costello et al. 2012)? Or perhaps a “metaorganism” / “supraorganism” (Bosch and McFall-Ngai 2011; Nicholson et al. 2012)? Alternatively,does the holobiont render the very notion of a biological individual untenable (Gilbert, Sapp and Tauber 2012)?

To address these questions, it is instrumental to offer an in-depth analysis of the kind of metabolic interactions that can characterize an individual organism,and to determine whether the interactions between the microbiota and the host are part of these metabolic interactions (in contrast to a situation in which, for instance, the microbiota would have with the host only very limited interactions in space and time).

Overall, this IDEM sub-project asks the following questions:

  • What is the history of the notions of symbiosis, mutualism,microbiotaand holobiont?
  • How do microorganisms enter into contact with their host, and through which mechanisms do they influence its development and its physiology?
  • Does the “holobiont” constitute an individual, a community, or an ecosystem? Does the concept of a holobiontinvalidate the notion of a biological individual?


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