Chlamydia; Endosymbiosis; Mitochondria; Ménage à trois hypothesis; Plastids; Rickettsiales; Symbiosis/physiology; Mitochondria/metabolism; Mitochondria/microbiology; Plastids/metabolism; Plastids/microbiology; Animals; Bacteria/metabolism; Bacteria/pathogenicity; Organelles/metabolism; Organelles/microbiology; Bacterial Physiological Phenomena; Bacteria; Organelles; Symbiosis; Medicine (all); Immunology and Microbiology (all); Biochemistry, Genetics and Molecular Biology (all); Agricultural and Biological Sciences (all)
Abstract :
[en] Endosymbionts are very common in nature, offering multiple occasions to recapitulate events that have led to the generation of mitochondria and plastids. However, both these organelles are unique because they are thought to derive from two individual events that gave rise to all eukaryotes and the plastids in algae and plants (excluding Paulinella chromatophora), respectively. This review focuses on the differences and similarities existing between extant endosymbionts and the two major endosymbiont derived organelles: the mitochondria and plastids. Emphasis is put on recent developments that point to the major role of intracellular pathogens in the establishment of these organelles. We argue that metabolic integration of bacterial endosymbionts into mitochondria and plastids required an unusually high degree of preadaptation not shared by most extant endosymbionts. We propose that this was achieved by either recruiting intracellular bacterial pathogens as "helper genomes" providing needed gene products, or by selecting endosymbionts destined to become organelles directly from such obligate intracellular bacteria. [fr] Les endosymbiontes sont très répandus dans la nature, offrant de multiples occasions de reproduire les événements qui ont engendré les mitochondries et des plastes. Cependant, ces deux organites sont uniques, car ils sont supposés dériver de deux événements individuels qui ont donné naissance d’une part à tous les eucaryotes et d’autre part aux plastes dans les algues et les plantes (à l’exception de Paulinella chromatophora). Cette revue se concentre sur les différences et les similitudes existant entre les endosymbiontes actuels et les deux principaux organites dérivés des endosymbiontes : la mitochondrie et les plastes. L’accent est mis sur des découvertes récentes qui soulignent le rôle majeur des pathogènes intracellulaires dans l’établissement de ces organites. Nous défendons l’idée que l’intégration métabolique des endosymbiontes bactériens dans les mitochondries et les plastes a nécessité un degré exceptionnellement élevé de préadaptation dont sont dépourvus la plupart des endosymbiontes actuels. Nous proposons que cela se soit réalisé soit en recrutant des bactéries pathogènes intracellulaires apportant les fonctions indispensables au succès de l’endosymbiose, soit en sélectionnant les endosymbiontes destinés à devenir des organites directement à partir de ces bactéries intracellulaires obligatoires.
Ball, Steven ; Unité de Glycobiologie Structurale et Fonctionnelle UMR8576, CNRS, Université de Lille, Villeneuve d’Ascq, France
Baurain, Denis ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes ; Laboratoire de Phylogénomique des Eucaryotes Bât, Belgium
Leleu, Marie ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes ; Unité de Glycobiologie Structurale et Fonctionnelle UMR8576, CNRS, Université de Lille, Villeneuve d’Ascq, France ; Laboratoire de Phylogénomique des Eucaryotes Bât, Belgium
Lafontaine, Ingrid ; Unité de Biologie du chloroplaste et perception de la lumière chez les micro-algues UMR7141 CNRS, Sorbonne Université, Institut de Biologie Physico-Chimique, Paris, France
Cenci, Ugo ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues ; Unité de Glycobiologie Structurale et Fonctionnelle UMR8576, CNRS, Université de Lille, Villeneuve d’Ascq, France
Colleoni, Christophe ; Unité de Glycobiologie Structurale et Fonctionnelle UMR8576, CNRS, Université de Lille, Villeneuve d’Ascq, France
Vallon, Olivier ; Unité de Biologie du chloroplaste et perception de la lumière chez les micro-algues UMR7141 CNRS, Sorbonne Université, Institut de Biologie Physico-Chimique, Paris, France
Greub, Gilbert ; Institut de microbiologie de l’Université de Lausanne, Département des laboratoires Bureau IMUL, Lausanne, Switzerland
Weber, Andreas ; Institute for Plant Biochemistry, Heinrich-Heine-University, Duesseldorf, Germany
Bhattacharya, Debashish ; Department of Biochemistry and Microbiology, Rutgers, The State University of New Jersey, New Brunswick, United States
Language :
English
Title :
Obligate intracellular bacterial pathogens as major players in the metabolic integration of organelles.
Keywords. Endosymbiosis, Mitochondria, Plastids, Chlamydia, Rickettsiales, M\u00E9nage \u00E0 trois hypothesis. Funding. CNRS, Universit\u00E9 de Lille CNRS, ANR grants \u201CMathtest\u201D (ANR-18-CE13-0027) \u201Cexpendo\u201D (ANR-14-CE11-0024) and \u201Cm\u00E9nage \u00E0 trois\u201D (ANR-12-BSV2-0009), R\u00E9gion Hauts de France and European project Alibiotech, ANR grant \u201CMathtest\u201D (ANR-18-CE13-0027). Note. Steven Ball is the recipient of the 2022 George Morel prize.SGB, UC, ML, and CC were supported by the CNRS, the Universit\u00E9 de Lille CNRS, the ANR grants \u201CMath-test\u201D (ANR-18-CE13-0027) \u201Cexpendo\u201D (ANR-14-CE11-0024) and \u201Cm\u00E9nage \u00E0 trois\u201D (ANR-12-BSV2-0009) and the R\u00E9gion Hauts de France and European project Alibiotech. UC, SGB, CC acknowledge BILILLE to provide computational resources. IL and OV were supported by ANR grant \u201CMathtest\u201D (ANR-18-CE13-0027).
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