Modulation of prey size reveals adaptability and robustness in the cell cycle of an intracellular predator

Santin, Yoann G.; Lamot, Thomas; Raaphorst, Renske van; Kaljević, Jovana; Laloux, Géraldine

doi:10.1016/j.cub.2023.04.059

Cited by 11 publications

(13 citation statements)

References 38 publications

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“…Furthermore, the quantification of offspring number showed that B. exovorus produces "fixed" numbers of progenies, typically three and less frequently two, irrespective of the prey size. This contrasts with the behaviour of the closely related endobiotic predatory bacterium B. bacteriovorus, which adjusts its growth phase to prey variability, resulting in the scaling of progeny number with prey cell size 32 . It is conceivable that growing inside a prey provides a protective nest enabling the exploitation of all available prey resources, if the predator can adjust its cell cycle to the variability of the prey -which is the case with B. bacteriovorus.…”

Section: Discussionmentioning

confidence: 83%

“…Our data suggest that the type of predation could also impact the feeding profile of the prey. Unlike B. bacteriovorus, which does not seem to require prey IM disruption for feeding (a shrinking but clearly defined prey cytoplasm can be seen throughout the predator growth phase; e.g., 31,32,37 ), predation by B. exovorus quickly results in the loss of prey IM integrity, possibly facilitating digestion and/or import of nutrients from the cytoplasm. Our results also suggest that the prey cellular content is digested in situ by B. exovorus.…”

Section: Discussionmentioning

confidence: 99%

“…The closely related endobiotic predator B. bacteriovorus, which grows inside its prey bacterium, uses non-binary division to produce odd or even progeny numbers, with reports of 2 to 17 daughter cells released per generation [32][33][34] . We recently established that B. bacteriovorus progeny numbers are determined by the size of the prey cell in which they grow 32 , which led us to assess if the apparent restricted variability in B. exovorus daughter cell numbers is explained by the relatively fixed C. crescentus cell size. Strikingly, comparable distributions of offspring numbers were measured (Fig.…”

Section: The Number Of B Exovorus Progenies Is Not Determined By Prey...mentioning

confidence: 99%

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Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Santin,

Sogues,

Bourigault

et al. 2023

Preprint

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Predatory bacteria feed upon and kill other bacteria in various natural environments. Obligate epibiotic predators like Bdellovibrio exovorus consume their prey whilst remaining attached to the outside of the prey. How these predators achieve epibiotic feeding through the prey cell envelope has not been explored previously. Whereas the S-layer is the only proposed defensive structure against predatory bacteria, it remains unclear how this thin outer layer of the envelope might prevent epibiotic attacks. Similarly, the lifecycle of B. exovorus during the predator-prey interaction is poorly understood, with current models suggesting a binary division. Here we imaged the entire predatory lifecycle of B. exovorus and the fate of its Caulobacter crescentus prey by time-lapse microscopy and cryo-electron microscopy to monitor predator attack, growth and division and assess the impact of the S-layer on epibiotic predation. Our data reveal that B. exovorus uses non-binary division in a novel proliferation pattern that mainly generates three progenies. Moreover, we found that B. exovorus predates regardless of the presence of an S-layer, calling for revisiting its protective role against predators. Finally, our results indicate that epibiotic predation relies on the establishment of a secured junction between the prey and predator outer membranes, which must be resolved unilaterally to maintain cellular integrity of the predator departing from the prey surface.

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Section: Discussionmentioning

confidence: 83%

Section: Discussionmentioning

confidence: 99%

Section: The Number Of B Exovorus Progenies Is Not Determined By Prey...mentioning

confidence: 99%

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Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Santin,

Sogues,

Bourigault

et al. 2023

Preprint

Self Cite

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show abstract

“…The closely related endobiotic predator B. bacteriovorus , which grows inside its prey bacterium, uses non-binary division to produce odd or even progeny numbers, with reports of 2 to 17 daughter cells released per generation 32 – 34 . We recently established that B. bacteriovorus progeny numbers are determined by the size of the prey cell in which they grow 32 , which led us to assess if the apparent restricted variability in B. exovorus daughter cell numbers is explained by the relatively fixed C. crescentus cell size. Strikingly, comparable distributions of offspring numbers were measured (Fig.…”

Section: Resultsmentioning

confidence: 99%

Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Santin,

Sogues,

Bourigault

et al. 2024

Nat Commun

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Predatory bacteria feed upon other bacteria in various environments. Bdellovibrio exovorus is an obligate epibiotic predator that attaches on the prey cell surface, where it grows and proliferates. Although the mechanisms allowing feeding through the prey cell envelope are unknown, it has been proposed that the prey’s proteinaceous S-layer may act as a defensive structure against predation. Here, we use time-lapse and cryo-electron microscopy to image the lifecycle of B. exovorus feeding on Caulobacter crescentus. We show that B. exovorus proliferates by non-binary division, primarily generating three daughter cells. Moreover, the predator feeds on C. crescentus regardless of the presence of an S-layer, challenging its assumed protective role against predators. Finally, we show that apparently secure junctions are established between prey and predator outer membranes.

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“…The long-held requirement for filamentous growth and division has been challenged by observations with smaller Proteus mirabilis prey (< 2 µm), that reveal a remarkable shift to binary fission -this is accompanied by a requirement to remodel the old flagellar pole into a new invasion pole [61]. Additionally, progeny number can be conclusively linked to prey cell size [62], and the origin of replication is always located at the non-flagellated invasive pole [63].…”

Section: Observation Different Scalesmentioning

confidence: 99%

Moving toward a better understanding of the model bacterial predator Bdellovibrio bacteriovorus

Caulton

Lovering

2023

Microbiology

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The bacterial predator Bdellovibrio bacteriovorus is a model for the wider phenomenon of bacteria:bacteria predation, and the specialization required to achieve a lifestyle dependent on prey consumption. Bdellovibrio bacteriovorus is able to recognize, enter and ultimately consume fellow Gram-negative bacteria, killing these prey from within their periplasmic space, and lysing the host at the end of the cycle. The classic phenotype-driven characterization (and observation of predation) has benefitted from an increased focus on molecular mechanisms and fluorescence microscopy and tomography, revealing new features of several of the lifecycle stages. Herein we summarize a selection of these advances and describe likely areas for exploration that will push the field toward a more complete understanding of this fascinating ‘two-cell’ system.

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Modulation of prey size reveals adaptability and robustness in the cell cycle of an intracellular predator

Cited by 11 publications

References 38 publications

Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Lifecycle of a predatory bacterium vampirizing its prey through the cell envelope and S-layer

Moving toward a better understanding of the model bacterial predator Bdellovibrio bacteriovorus

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