Cell-cycle progress in obligate predatory bacteria is dependent upon sequential sensing of prey recognition and prey quality cues

Rotem, Or; Pasternak, Zohar; Shimoni, Eyal; Belausov, Eduard; Porat, Ziv; Pietrokovski, Shmuel; Jurkevitch, Édouard

doi:10.1073/pnas.1515749112

Cited by 47 publications

(50 citation statements)

References 80 publications

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“…Moreover, a regulatory protein hub controlling predatory invasion was discovered at this pole (38). The pili protruding from the invasive pole take part in sequentially sensing the stepwise phase transition in B. bacteriovorus (38, 39). During prey recognition, the pili mediate the transduction of a yet-unidentified early signal that occurs in the cytoplasmic membrane of the host (38).…”

Section: Discussionmentioning

confidence: 99%

“…During prey recognition, the pili mediate the transduction of a yet-unidentified early signal that occurs in the cytoplasmic membrane of the host (38). The second cue, which also has not yet been specified, originates from the prey cytoplasm and is believed to promote DNA replication (39). Thus, the invasive pole of B. bacteriovorus seems to be involved in the transition from the attack phase to the reproductive phase.…”

Section: Discussionmentioning

confidence: 99%

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Dynamics of chromosome replication and its relationship to predatory attack lifestyles in Bdellovibrio bacteriovorus

Makowski

Trojanowski

Till

et al. 2019

Preprint

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13Bdellovibrio bacteriovorus is a small Gram-negative, an obligate predatory bacterium that is 14 largely found in wet, aerobic environments (i.e. soil). This bacterium attacks and invades other 15 Gram-negative bacteria, including animal and plant pathogens. The intriguing life cycle of B. 16 bacteriovorus consists of two phases: a free-living non-replicative attack phase wherein the 17 predatory bacterium searches for its prey, and a reproductive phase, in which B. bacteriovorus 18 degrades a host's macromolecules and reuses them for its own growth and chromosome 19 replication. Although the cell biology of this predatory bacterium has gained considerable 20 interest in recent years, we know almost nothing about the dynamics of chromosome replication 21 in B. bacteriovorus. Here, we performed a real-time investigation into the subcellular 22 localization of the replisome(s) in single cells of B. bacteriovorus. Our results confirm that in 23 B. bacteriovorus chromosome replication fires only during the reproductive phase, and show 24 for the first time that this predatory bacterium exhibits a novel spatiotemporal arrangement of 25 chromosome replication. The replication process starts at the invasive pole of the predatory 26 bacterium inside the prey cell and proceeds until several copies of the chromosome have been 27 completely synthesized. This chromosome replication is not coincident with the predator-cell 28 division, and it terminates shortly before synchronous predator-filament septation occurs. In 29 addition, we demonstrate that if this lifecycle fails in some cells of B. bacteriovorus, they can 30 instead use two prey cells sequentially to complete their life cycle. 31 Importance 32 New strategies are needed to combat multidrug-resistant bacterial infections. Application of the 33 predatory bacterium, Bdellovibrio bacteriovorus, which kills other bacteria including 34 pathogens, is considered promising for bacterial infections. The B. bacteriovorus life cycle 35 consists of two phases, a free-living, invasive attack phase and an intracellular reproductive 36 phase, in which this predatory bacterium degrades the host's macromolecules and reuses them 37 3 for its own growth. To understand the use of B. bacteriovorus as a 'living antibiotic', it is first 38 necessary to dissect its life cycle including chromosome replication. Here, we present for the 39 first time a real-time investigation into subcellular localization of chromosome replication in a 40 single cells of B. bacteriovorus. This process initiates at the invasion pole of B. bacteriovorus 41 and proceeds until several copies of the chromosome have been completely synthesized. 42 Interestingly, we demonstrate that some cells of B. bacteriovorus require two prey cells 43 sequentially to complete their life cycle. 44 45Bdellovibrio bacteriovorus is a small (0.2-to 0.5-μm wide and 0.5-to 2.5-μm long) 46 Gram-negative bacterium that is unusual in its ability to invade and kill other Gram-negative 47 bacteria. Moreover, it was demonstrated th...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Dynamics of chromosome replication and its relationship to predatory attack lifestyles in Bdellovibrio bacteriovorus

Makowski

Trojanowski

Till

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Ces phases sont morphologiquement, spatialement, physiologiquement et transcriptionnellement très différentes. S'y ajoute une phase transitoire (PT) qui a été récemment décrite [14]. Une division supplémentaire de ces étapes dépend de la stratégie prédatrice adoptée.…”

Section: Le Cycle Cellulaire Des Bdellovibrio Et Organismes Apparentésunclassified

“…Très récemment, l'existence entre PA et PC d'une phase discrète du cycle cellulaire [14] a été démontrée. Un système de croissance de souches sauvages de B. bacteriovorus (donc incapables de croissance axénique 7 ) sur des bactéries proies d'Escherichia coli, vidées de leur contenu cytoplasmique, a été développé.…”

Section: La Phase Transitoireunclassified

“…La PT apparaît comme un point de contrôle du cycle cellulaire où la décision de s'engager dans la croissance est liée à la détection du signal cytoplasmique. Celui-ci pourrait servir d'indicateur de la valeur nutritionnelle de la proie, afin d'empêcher l'entrée en PC en l'absence des ressources nécessaires à la complétion du cycle de reproduction [14]. Certains processus considérés jusqu'à présent comme faisant partie de la PC sont en fait caractéristiques de la PT.…”

Section: La Phase Transitoireunclassified

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Bdellovibrioet organismes apparentés

Jurkevitch¹,

Jacquet²

2017

Med Sci (Paris)

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> Les bactéries prédatrices obligatoires d'autres bactéries, les bactéries nécessitant une cellule proie Gram négatif afin de compléter leur cycle cellulaire, appartiennent au groupe polyphylétique des Bdellovibrio et organismes apparentés (BALO). Bien que les interactions entre les bactéries prédatrices et les bactéries proies soient complexes, leur dynamique et leur impact sur les communautés bacté-riennes dans l'environnement commencent à être compris. Les BALO ont des cycles de vie particuliers : ils grandissent soit de manière épibiotique, quand le prédateur reste attaché à l'enveloppe de sa proie, la division cellulaire étant alors binaire, ou ils se développent dans le périplasme de la cellule proie. Dans ce cas, un prédateur génère plusieurs cellules. Le cycle de vie périplasmique exprime des motifs d'expression géniques et protéiques ainsi que des réseaux de signalisation uniques. Cette revue explore quelques particularités de l'écologie et de la biologie cellulaire des BALO, ainsi que leurs applications potentielles dans les domaines médicaux, agricoles et environnementaux. < like organisms (BALO) qui inclue divers groupes monophylétiques : le genre Micavibrio et les familles Bdellovibrionaceae, Bacteriovoraceae et Peridibacteraceae [2]. Ces BALO ont pour cible des bactéries Gram négatif. La pression de prédation, pouvant conduire à la sélection de proies génétiquement résistantes, et l'existence de défenses phénoty-piques et de nature transitoire, qui constituent un mécanisme d'amortissement, assurent, in fine, à la fois la survie du prédateur et la capacité de la proie à se reconstituer [3,4]. La dynamique des relations de type proie-prédateur entre bactéries s'avère donc complexe. S'ajoute à cette complexité, la nature mal définie du type d'interaction possible entre organismes (synergique, antagoniste, etc.). Cependant, les nouvelles technologies de séquençage, de bio-informatique et de microscopie, mais aussi le développement d'outils de manipulation génétique, permettent, aujourd'hui, une étude détaillée des méca-nismes cellulaires qui font d'une bactérie, un prédateur obligatoire. Elles offrent également une approche plus large de l'étude de leur impact écologique. Ces connaissances ouvrent de nouvelles voies vers leur application en agriculture, en aquaculture, dans la préservation de notre environnement et en médecine. Cette revue est l'occasion de synthétiser une partie des connaissances actuelles sur les BALO. Le monde méconnu des BALOOn sait aujourd'hui que les BALO sont très largement distribués au sein de la biosphère et sont présents aussi bien dans les océans, les mers, les eaux côtières, les estuaires, les rivières, les lacs, que dans les bassins d'aquaculture, les stations d'épuration, l'eau d'irrigation, ou encore dans les sols, les rizières, la rhizosphère et même dans les

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An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

et al. 2017

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The transition to multicellularity, recognized as one the major transitions in evolution, has occurred independently several times. While multicellular development has been extensively studied in zygotic organisms including plant and animal groups, just a few aggregative multicellular organisms have been employed as model organisms for the study of multicellularity. Studying different evolutionary origins and modes of multicellularity enables comparative analyses that can help identifying lineage-specific aspects of multicellular evolution and generic factors and mechanisms involved in the transition to multicellularity. Among aggregative multicellular organisms, myxobacteria are a valuable system to explore the particularities that aggregation confers to the evolution of multicellularity and mechanisms shared with clonal organisms. Moreover, myxobacteria species develop fruiting bodies displaying a range of morphological diversity. In this review, we aim to synthesize diverse lines of evidence regarding myxobacteria development and discuss them in the context of Evo-Devo concepts and approaches. First, we briefly describe the developmental processes in myxobacteria, present an updated comparative analysis of the genes involved in their developmental processes and discuss these and other lines of evidence in terms of co-option and developmental system drift, two concepts key to Evo-Devo studies. Next, as has been suggested from Evo-Devo approaches, we discuss how broad comparative studies and integration of diverse genetic, physicochemical, and environmental factors into experimental and theoretical models can further our understanding of myxobacterial development, phenotypic variation, and evolution.

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Cell-cycle progress in obligate predatory bacteria is dependent upon sequential sensing of prey recognition and prey quality cues

Cited by 47 publications

References 80 publications

Dynamics of chromosome replication and its relationship to predatory attack lifestyles in Bdellovibrio bacteriovorus

Dynamics of chromosome replication and its relationship to predatory attack lifestyles in Bdellovibrio bacteriovorus

Bdellovibrioet organismes apparentés

An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

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