Motility Control of Symbionts and Organelles by the Eukaryotic Cell: The Handling of the Motile Capacity of Individual Parts Forges a Collective Biological Identity Guglielmo Militello To cite this version: Guglielmo Militello. Motility Control of Symbionts and Organelles by the Eukaryotic Cell: The Handling of the Motile Capacity of Individual Parts Forges a Collective Biological Identity. Frontiers in Psychology, Frontiers, 2019, 10, 10.3389/fpsyg.2019.02080. hal-02338090 HAL Id: hal-02338090 https://hal.archives-ouvertes.fr/hal-02338090 Submitted on 29 Oct 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. HYPOTHESIS AND THEORY published: 10 September 2019 doi: 10.3389/fpsyg.2019.02080 Motility Control of Symbionts and Organelles by the Eukaryotic Cell: The Handling of the Motile Capacity of Individual Parts Forges a Collective Biological Identity Guglielmo Militello* Department of Logics and Philosophy of Science, IAS-Research Centre, University of the Basque Country, San Sebastián, Spain Motility occupies a decisive role in an organism’s ability to autonomously interact with its environment. However, collective biological organizations exhibit individual parts, which have temporally or definitively lost their motor capacities, but still able to autonomously interact with their host. Indeed, although the flagella of bacterial symbionts of eukaryotic cells are usually inhibited or lost, they autonomously modify the environment provided by their host. Furthermore, the eukaryotic organelles of endosymbiotic origin (i.e., mitochondria and plastids) are no longer able to move autonomously; nonetheless, they make a cytoskeletal-driven motion that allows them to communicate with other eukaryotic cells Edited by: Luisa Damiano, and to perform a considerable number of physiological functions. The purpose of this University of Messina, Italy article is twofold: first, to investigate how changes in the motile capacities of the parts of Reviewed by: a nested biological organization affect their interactive autonomy; second, to examine Fred Keijzer, University of Groningen, Netherlands how the modification of the interactive autonomy of the individual parts influences the Lynn Chiu, constitutive autonomy of the collective association as a whole. The article argues that the Université de Bordeaux, France emergence and maintenance of collective biological identities involves a strict control of *Correspondence: the motile abilities of their constituting members. This entails a restriction, but not Guglielmo Militello [email protected] necessarily a complete loss, of the agential capacities of the individual parts. Specialty section: Keywords: motility, interactive autonomy, constitutive autonomy, eukaryotic cell, collective biological identity, This article was submitted to symbionts, mitochondria, plastids Theoretical and Philosophical Psychology, a section of the journal INTRODUCTION Frontiers in Psychology Received: 05 May 2019 By collective (or nested) biological organizations, we mean biological entities consisting of different Accepted: 27 August 2019 parts, each having their own genetic and phenotypic identity. Symbiotic associations and ecosystems Published: 10 September 2019 are pre-eminently examples of nested organizations, as the biological members of these associations Citation: exhibit distinct genomes and specific phenotypic features. The eukaryotic cell is now a unique Militello G (2019) Motility Control of functionally integrated individual, but its evolutionary origin dates to two (so far proven) Symbionts and Organelles by the endosymbiotic events: the endosymbiosis between an α-proteobacterium and the proto-eukaryotic Eukaryotic Cell: The Handling of the Motile Capacity of Individual Parts cell is at the origin of mitochondria, whereas the endosymbiosis between a cyanobacterium Forges a Collective Biological Identity. and the proto-eukaryotic cell gave rise to plastids. Accordingly, eukaryogenesis is currently Front. Psychol. 10:2080. explained as a progressive transformation of a nested biological organization into a functionally doi: 10.3389/fpsyg.2019.02080 integrated individual that still saves some traces of its symbiotic past (Martin et al., 2015). Frontiers in Psychology | www.frontiersin.org 1 September 2019 | Volume 10 | Article 2080 Militello Motility Control Symbionts and Organelles The interaction among the members of a collective association the integration of closely related units (i.e., eukaryotic organelles). is complex and includes a variety of processes ranging from Furthermore, the different interactive behaviors of symbionts metabolic fluxes to chemical signals involved in coordinated and organelles will shed light on their different organizational gene expression. An important, yet neglected, aspect of nested roles within the eukaryotic cell and explain why they are associations is the motility of their parts, because the motile differently controlled. capacities of components are severely constrained by the whole The article is divided as follows: in section “Interactions as association. Since a living being can reach its nutrients in the the Cornerstone of Symbiotic Associations and Autonomous environment and interact with its surroundings by means of Organisms”, we present a critical review of the current debate motile capacities, the way in which motility is controlled and on the individuality of symbiotic associations and some theoretical constrained affects the biological capacities not only of the accounts of the relationship between “interactive” and parts but also of the collective association as a whole. “constitutive” autonomy. The following two sections will examine This article aims at exploring how the constraints imposed the physical constraints acting on the motility of eukaryotic on the motility of the individual parts (i.e., symbionts and symbionts (section “The Control of Symbiotic Motility”) and organelles) of an eukaryotic cell affect their autonomous eukaryotic organelles (section “Mobility of Eukaryotic interactive capacities and at evaluating how this affects the Organelles”). Section “Interactive Dynamics and the constitutive autonomy of the overall collective association. Organizational Role of the Eukaryotic Cytoskeleton” will explore Accordingly, the key question of this article can be stated as the role played by the eukaryotic cytoskeleton in the control follows: how can a collective identity emerge from the control of motility and the evolutionary innovations that it has introduced. and transformation of the motility of the individual parts? Finally, section “Concluding Remarks: The Relationship Between In order to address this issue, we will analyze how the Motility and Biological Autonomy” makes some concluding motility of the symbionts of the eukaryotic cell is controlled remarks concerning the relationship between motility and by the host so as to1 enable the self-maintenance of the whole biological autonomy. symbiotic association. The control of motility occupies a decisive role not only in ongoing symbiotic associations but also in the transformation of endosymbiotic proto-mitochondria and INTERACTIONS AS THE CORNERSTONE proto-plastids into eukaryotic organelles: indeed, the eukaryotic OF SYMBIOTIC ASSOCIATIONS AND cytoskeleton tightly controls the movement of eukaryotic AUTONOMOUS ORGANISMS organelles in such a way that physiological functions and homeostatic regulatory mechanisms can be performed. Over the past years, an increasing number of studies have Accordingly, from an evolutionary point of view, the eukaryotic stressed the cardinal importance of symbiotic interactions for cytoskeleton has introduced biological novelties that permitted defining a biological individual. The eukaryotic cell, notably a proto-eukaryotic cell and its endosymbionts to achieve a in multicellular organizations, forms a nested ecosystem with functionally integrated individuality. their bacterial symbionts in such a way that they form a unique In the light of the above, the main issue of this article will collective identity based on their mutual interactions (McFall- be explored by addressing the following theoretical questions: Ngai et al., 2013). Although the term “holobiont” currently designates the relationship between a multicellular eukaryote 1. How is the motility of symbionts controlled by the host with its bacterial symbionts, Margulis (1993) employed this so as to enable the self-maintenance of the overall term to refer to a general symbiotic association between a symbiotic association? symbiont and a host. The variety of symbiotic associations is 2. How is the motility of eukaryotic organelles controlled extremely wide, since they range from prokaryote-prokaryote by cytoskeleton? interactions [e.g., the Candidatus Tremblaya princeps-Candidatus 3. What is the role played by the eukaryotic cytoskeleton in Moranella endobia consortium of Planococcus citri (McCutcheon controlling the interactive capacities of endosymbionts and and von Dohlen, 2011) or the bacterial