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Zoom Sur Les Bdellovibrio Et Organismes Apparentés (Balos) Notes Académiques de l'Académie d'agriculture de France Academic Notes from the French Academy of Agriculture (N3AF) Note de synthèse Bactéries prédatrices : zoom sur les Bdellovibrio et organismes apparentés (BALOs) Jade A. Ezzedine1, Stéphan Jacquet1 1 Université Savoie Mont-Blanc, Inra, UMR CARRTEL, 75 bis avenue de Corzent, 74200 Thonon-les-Bains, France Correspondance : [email protected] Résumé Cette revue décrit un groupe bactérien lève le voile sur ce groupe bactérien et leur fonctionnel unique, les Bdellovibrio et place dans les systèmes naturels, et explore organismes apparentés, ou BALOs leurs applications pour améliorer le bien-être (Bdellovibrio and like organisms). Ces humain et animal face à des pathogènes de bactéries Gram négatif sont des prédateurs plus en plus résistants aux antibiotiques de obligatoires d’autres bactéries, caractérisés synthèse. par diverses stratégies de prédation, un spectre de prédation large permettant de faire face à tout type de compétitivité, et un cycle Abstract de vie garantissant une multiplication très This review describes a unique functional efficace. Ce groupe pourrait remplir un rôle bacterial group referred to as Bdellovibrio and écologique tout aussi primordial que celui des like organisms (BALOs). These gram-negative bactériophages en ce qui concerne le bacteria are obligate predators of other bacteria, contrôle des populations bactériennes. with, on one hand, different predation strategies, Agents biologiques efficaces et alternative a remarkable predation spectrum to cope with prometteuse à l’utilisation des antibiotiques any type of competitiveness, as well as a de synthèse, les bactéries prédatrices sont competent life cycle ensuring efficient considérées dans de nombreuses multiplication. On the other hand, this group applications relevant de la médecine et des could fulfill a similar ecological role as biotechnologies. Cependant, avant de bacteriophages concerning the control of compter définitivement sur ces organismes bacterial populations. As potentially important pour nous guérir, ils doivent encore faire leurs natural bioagents, they are more and more preuves dans des systèmes in vivo considered as alternatives to antibiotics and are complexes et non contrôlés, à l’inverse des investigated for potential uses in medicine and milieux de culture de laboratoire. Cette revue biotechnologies. However, before relying on Notes Académiques de l'Académie d'agriculture de France (N3AF) 2019, 2, 1-25 1 Notes Académiques de l'Académie d'agriculture de France Academic Notes from the French Academy of Agriculture (N3AF) Note de synthèse them to help and heal us, their role in complex spécialistes de ce groupe s’accordent plutôt à and uncontrolled in vivo systems needs to be les définir comme des prédateurs, car ces experimentally assessed, unlike classic broth derniers mettent fin à l’activité métabolique de medium in the laboratory. This review uncovers leur hôte en induisant la mort de leur proie dans what lies behind this group and explores their les 15 minutes suivant l’infection (Chen et place in natural systems as well as their Williams, 2012). Et comme tout prédateur dont le applications to improve human and animal besoin est de se nourrir, les BALOs entament à wellbeing against pathogens increasingly resistant nouveau une recherche dynamique de nouvelles to antibiotics. proies, ce qui les différencie des « parasites » sensu stricto (voir le Complément électronique 1). Si les BALOs ne sont pas les seuls Mots clés prédateurs bactériens connus (Complément Bdellovibrio, BALOs, bioagents, prédateur, électronique 2), ils sont les plus étudiés (Harini applications et al., 2013). Malgré une distribution qui semble ubiquiste Keywords et, donc, un rôle fonctionnel supposé Bdellovibrio, BALOs, bioagent, predator, important ou avéré dans certains cas, très applications peu d’études ont été consacrées au rôle et à l’impact de ces prédateurs sur la communauté bactérienne des Introduction environnements naturels et anthropisés. Les interactions biotiques qui ont été très étudiées Les microorganismes (virus, bactéries, archées, pour les bactéries ont surtout été celles eucaryotes unicellulaires (« protistes »)…) sont impliquant les virus de bactéries (phages ou abondants, diversifiés, ubiquistes et ont des rôles bactériophages) et les protistes nanoflagellés. importants dans le fonctionnement des En effet, il a souvent été décrit que les écosystèmes. L'écologie microbienne vise à bactériophages et les protistes contribuent étudier la diversité et les interactions entre ces majoritairement à la mortalité bactérienne et au microorganismes, et également entre ces derniers renouvellement de cette communauté au sein et leur environnement abiotique. Il existe de des écosystèmes aquatiques (Miki et Jacquet, nombreuses interactions biotiques (qui relèvent 2010). Cependant certains auteurs avancent de la prédation, du parasitisme, etc.) ; parmi aujourd’hui que cette affirmation pourrait être celles-ci, certaines ont encore été très peu revue à la baisse. En effet, bien que les virus explorées. C’est le cas pour un groupe restent à ce jour l’entité biologique la plus remarquable de prédateurs bactériens nommé abondante de la biosphère, leur concentration a Bdellovibrio et organismes apparentés, connu vraisemblablement été surestimée, notamment sous l’acronyme anglo-saxon BALOs pour suite à la découverte des vésicules Bdellovibrio And Like Organisms. Les BALOs membranaires extracellulaires qui se confondent (Figure 1) sont des bactéries Gram négatif, avec les virus (Gaudin et al., 2014 ; Soler et al., prédateurs obligatoires d’autres bactéries. Dans 2015). la majorité des cas, le prédateur se loge dans sa Cette synthèse présente les BALOs et montre proie (ou hôte) pour former une chambre appelée leur importance dans les écosystèmes « bdelloplaste » qui lui permet de (1) digérer à microbiens. l’abri le contenu cellulaire de sa proie, (2) se développer sous la forme d’une cellule filamenteuse, et, in fine, (3) donner naissance à Caractéristiques générales des BALOs plusieurs « progénitures ». On pourrait parler de parasitoïdes pour ces cellules, mais les La découverte des BALOs est le fruit accidentel Notes Académiques de l'Académie d'agriculture de France (N3AF) 2019, 2, 1-25 2 Notes Académiques de l'Académie d'agriculture de France Academic Notes from the French Academy of Agriculture (N3AF) Note de synthèse des recherches menées dans les années 1960 de Bdellovibirio (Stolp et Petzold, 1962 ; Stolp et par Stolp dédiées initialement à l’isolement des Starr, 1963). Ce mot dérive de Bdella, signifiant bactériophages du phytopathogène Pseudo- sangsue en grec. En effet, le BALO s’attache à monas syringae pv. phaseolicola, l’agent sa proie, y pénètre ou non selon l’espèce, et responsable de la graisse du haricot. En absorbe tel un vampire le contenu cellulaire de compagnie de Petzold et Starr, Stolp décrivit et sa victime (Harini et al., 2013). Découverts désigna ce groupe de micro-organismes formant initialement dans le sol, puis dans des milieux des plaques autour de bactéries sous le vocable variés tels que les environnements lacutres et Figure 1. Images de microscopie électronique à transmission et à balayage montrant différents BALOs à l’état planctonique et en phase de prédation. A) Micavibrio sp. et B) Bdellovibrio bacteriovorus 109J (extrait de Davidov et al., 2006); C) Halobacteriovorax sp. (source Welsh et al., 2016); D) Bacteriovorax stolpii (source Richards et al., 2012); E) Formation d’un bdelloplaste (prédation endobiotique) (source Chen et al., 2015); F) B. exovorus associé à sa proie (prédation épibiotique) (source Rotem et al., 2014). Notes Académiques de l'Académie d'agriculture de France (N3AF) 2019, 2, 1-25 3 Notes Académiques de l'Académie d'agriculture de France Academic Notes from the French Academy of Agriculture (N3AF) Note de synthèse marins (Schwudke et al., 2001), les BALOs génération (NGS), dites aussi à haut débit, a semblent être partout où on les cherche. Les permis de franchir de nouvelles frontières dans BALOs à l’état planctonique (Figure 1) sont l’analyse des communautés bactériennes en uniflagellés et mobiles, souvent en forme de fournissant une grande quantité d’information vibroïde (Davidov et al., 2006; Williams et al., dans l’identification des phylotypes microbiens 2015). (Li et Williams, 2015). Leur comportement de prédation est gouverné Les NGS et les outils bio-informatiques ont par le locus hit (host interaction). Toutefois une relancé ou favorisé les études de génomique mutation spontanée de ce locus se traduit par la ciblée, autrement dit la métagénétique ou génération de BALOs hôte-indépendants (BALO- metabarcoding (étude d’un seul marqueur HI) capables de se répliquer par simple fission moléculaire), et de métagénomique (étude de binaire (Roschanski et al., 2011 ; Oyedara et al., l'ensemble du génome). La détection des BALOs 2016). Les BALOs ont été détectés et étudiés à peut ainsi se faire en se basant sur le l’origine par des méthodes de culture classiques séquençage du gène 16S (caractéristique des de laboratoire, avec leurs avantages, mais aussi procaryotes) codant la petite sous-unité des leurs limites : cultiver des bactéries a ribosomes (ARNr) mais aussi sur le gène de la généralement pour résultat de sous-estimer sous-unité bêta de l’ARN polymérase (rpoB) considérablement la diversité réelle. On rapporte (Pineiro et al., 2004). d’ailleurs souvent que seulement 1 % des micro- Aujourd’hui, suite aux remaniements réguliers de organismes
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