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Microorganisms as scaffolds of host individuality: an eco-immunity account of the holobiont

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Abstract

There is currently a great debate about whether the holobiont, i.e. a multicellular host and its residential microorganisms, constitutes a biological individual. We propose that resident microorganisms have a general and important role in the individuality of the host organism, not the holobiont. Drawing upon the Equilibrium Model of Immunity (Eberl in Nat Rev Immunol 16:524–532, 2016), we argue that microorganisms are scaffolds of immune capacities and processes that determine the constituency and persistence of the host organism. A scaffolding perspective accommodates the contingency and heterogeneity of resident microorganisms while accounting for their necessity and unifying contributions to host individuality. In our symbiotic view of life, holobionts may not be organisms or units of selection, but macroorganisms cannot persist nor function as individuals without their scaffolding microorganisms.

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Notes

  1. The term “macroorganism,” coined by O’Malley and Dupré (2007), refers to  multicellular beings that can accommodate a large number of microorganisms. Microorganisms, in turn, include a wide scope of taxa engaged in a broad range of symbiotic relations, e.g. mutualism, commensalism, parasitism, etc.

  2. See for instance, Margulis and Fester (1991), Dupré and O’Malley (2009), Bosch and McFall-Ngai (2011), Pradeu (2011), McFall-Ngai et al. (2013), Hutter et al. (2015), Gilbert and Epel (2016), Sapp (2016), Theis et al. (2016).

  3. See Zilber-Rosenberg and Rosenberg (2008), Gilbert et al. (2012), Bordenstein and Theis (2015), Lloyd (2017).

  4. See for instance, Turnbaugh et al. (2007), Zilber-Rosenberg and Rosenberg (2008), Gilbert et al. (2012), McFall-Ngai et al. (2013), Pradeu (2016), O’Malley (2014).

  5. Peter Godfrey-Smith pointed us to this reference in O’Malley (2016).

  6. Nevertheless, immunology is but one incomplete way to approach the overall roles of microorganisms in the life of the macroorganism host. Metabolic, evolutionary, and immunological considerations may churn out notions of individuality that cross-cut the holobiont.

  7. The names of the immune responses—Type 1, 2, 3—follow standard usage in immunology.

  8. Some key references: ecological developmental biology (Gilbert and Epel 2016), ecological physiology (Turner 2000), niche construction in behavior, ecology, and evolution (Odling-Smee et al. 2003; Sultan 2015); niche construction in developmental biology (Flynn et al. 2013), and eco-immunology (Demas and Nelson 2012).

  9. The balance between mutually inhibitory immune responses does not necessarily result in steady-state equilibria, but could also lead to oscillations or other dynamics. The main issue is that these dynamics are the consequences of microorganism regulation of immune responses, and that they promote the maintenance of host individuality. The focus on microorganism-induced dynamics at a higher level of organization is in line with studies on the high-level functional stability and low-level taxonomic variability of microorganism communities (Turnbaugh et al. 2009; Coyte et al. 2015; Taxis et al. 2015).

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Acknowledgements

We thank Thomas Pradeu for bringing us together during the first ERC-IDEM workshop at Bordeaux and for the multiple rounds of extremely valuable comments and discussions. We also thank the three anonymous referees for their rapid, insightful, and impressively detailed comments. Special thanks to Layal Massara, ChiaHua Lin, Richard Lauer, Scott Gilbert, Peter Godfrey-Smith, and the participants of the First Bordeaux-San Sebastian Workshop on Philosophy of Biology for their useful comments, and to Valérie Jolivel, Weijen Liu, Bi-Huei Yang, and André Ariew for encouraging discussions at various stages of this manuscript. We thank Gregory Dupuy for editorial suggestions. Part of this work was inspired by discussions with James Griesemer after ISHPSSB 2013. All mistakes and errors are exclusively our own. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme—grant agreement No 637647—IDEM.

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  1. ImmunoConcEpT Lab, UMR CNRS 5164, University of Bordeaux/CNRS, Bat 1B, RDC, 146 rue Léo Saignat, 33076, Bordeaux, France

    Lynn Chiu

  2. Microenvironment and Immunity Unit, INSERM U1224, Institut Pasteur, 25 rue du Dr Roux, 75724, Paris, France

    Gérard Eberl

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Chiu, L., Eberl, G. Microorganisms as scaffolds of host individuality: an eco-immunity account of the holobiont. Biol Philos 31, 819–837 (2016). https://doi.org/10.1007/s10539-016-9552-0

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