For the greater good: Programmed cell death in bacterial communities

Peeters, Stijn H.; Jonge, Marien I. de

doi:10.1016/j.micres.2017.11.016

Cited by 76 publications

(68 citation statements)

References 80 publications

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“…Conceivably, HGT mediated by the GTAs can confer additional metabolic or transport capacities to the recipient bacteria. Additionally, GTAs could be perceived as a mechanism bacterial programmed cell death (38,39). Under this type of adaptation, the GTA-mediated lysis of a fraction of the bacterial community would decrease the population density and increase the nutrient availability per cell, by supplying additional nutrients released from the lysed cells.…”

Section: Discussionmentioning

confidence: 99%

Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents

Kogay

Wolf

Koonin

et al. 2020

Preprint

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Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria. The GTAs can be induced under nutritional stress, incorporate random fragments of bacterial DNA into mini-phage particles, lyse the host cells and infect neighboring bacteria, thus enhancing horizontal gene transfer. We show that the GTA genes evolve under pronounced positive selection for the reduction of the energy cost of protein production as shown by comparison of the amino acid compositions with both homologous viral genes and host genes. The energy saving in GTA genes is comparable to or even more pronounced than that in the genes encoding the most abundant, essential bacterial proteins. In cases when viruses acquire genes from GTAs, the bias in amino acid composition disappears in the course of evolution, showing that reduction of the energy cost of protein is an important factor of evolution of GTAs but not bacterial viruses. These findings strongly suggest that GTAs are bacterial adaptations rather than selfish, virus-like elements. Because GTA production kills the host cell and does not propagate the GTA genome, it appears likely that the GTAs are retained in the course of evolution via kin or group selection. Therefore, we hypothesize that GTA facilitate the survival of bacterial populations under energy-limiting conditions through the spread of metabolic and transport capabilities via horizontal gene transfer and increase of nutrient availability resulting from the altruistic suicide of GTA-producing cells. ImportanceKin and group selection remain controversial topics in evolutionary biology. We argue that these types of selection are likely to operate in bacterial populations by showing that bacterial Gene Transfer Agents (GTAs), but not related viruses, evolve under positive selection for the reduction of the energy cost of a GTA particle production. We hypothesize that GTAs are dedicated devices for the survival of bacteria under the conditions of nutrient limitation. The benefits conferred by GTAs under nutritional stress appear to include horizontal dissemination of genes that could provide bacteria with enhanced capabilities for nutrient utilization and the increase of nutrient availability through the lysis of GTA-producing bacteria.

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Section: Discussionmentioning

confidence: 99%

Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents

Kogay

Wolf

Koonin

et al. 2020

Preprint

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“…Apoptosis or programmed cell death (PCD) is a well-established process in eukaryotic cells whose existence in prokaryotes has recently been accepted 56–58 . One of the instigators of PCD is the age-dependent accumulation of damaged cellular components and flaws in metabolic reactions.…”

Section: Resultsmentioning

confidence: 99%

“…The physiological alterations observed in ΔtasA null strain reflect a process of progressive cellular deterioration characteristic of senescence 56–58 , including early activation of secondary metabolism, low energy metabolic activity, and accumulation of damaged molecular machinery that is required for vital functions. Indeed, it has been previously demonstrated that such metabolic changes can trigger PCD in other bacterial species, in which over-acidification of the cytoplasm eventually leads to the activation of cell death pathways 54 .…”

Section: Discussionmentioning

confidence: 99%

Dual functionality of the TasA amyloid protein inBacillusphysiology and fitness on the phylloplane

Cámara-Almirón

Navarro

Magno-Pérez-Bryan

et al. 2019

Preprint

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AbstractBacteria can form biofilms that consist of multicellular communities embedded in an extracellular matrix (ECM). Previous studies have demonstrated that genetic pathways involved in biofilm formation are activated under a variety of environmental conditions to enhance bacterial fitness; however, the functions of the individual ECM components are still poorly understood. In Bacillus subtilis, the main protein component of the ECM is the functional amyloid TasA. In this study, we demonstrate that beyond their well-known defect in biofilm formation, ΔtasA cells also exhibit a range of cytological symptoms indicative of excessive cellular stress, including DNA damage accumulation, changes in membrane potential, higher susceptibility to oxidative stress, and alterations in membrane dynamics. Collectively, these events can lead to increased programmed cell death in the colony. We show that these major physiological changes in ΔtasA cells are likely independent of the structural role of TasA during amyloid fiber formation in the ECM. The presence of TasA in cellular membranes, which would place it in proximity to functional membrane microdomains, and mislocalization of the flotillin-like protein FloT in ΔtasA cells, led us to propose a role for TasA in the stabilization of membrane dynamics as cells enter stationary phase. We found that these alterations caused by the absence of TasA impair the survival, colonization and competition of Bacillus cells on the phylloplane. Taken together, our results allow the separation of two complementary roles of this functional amyloid protein: i) structural functions during ECM assembly and interactions with plants, and ii) a physiological function in which TasA, via its localization to the cell membrane, stabilizes membrane dynamics and supports more effective cellular adaptation to environmental cues.

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“…Due to nutrient and space limitations the cells can no longer grow and eventually stochastically die (14). However, recent evidences suggest that programmed cell death may be a viable strategy in prokaryotes (15)(16)(17). So, with this initial assumption we wanted to shed light on the mode of death during bacterial death phase.…”

Section: E Coli Death Phase Population Does Not Show Hallmarks Of Apmentioning

confidence: 99%

MazEF-rifampicin interaction suggests a mechanism for rifampicin induced inhibition of persisters

Alexander

Guru

Pradhan

et al. 2020

Preprint

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Background: Persistence is a natural phenomenon whereby a subset of a population of isogenic bacteria either grow slow or become dormant conferring them with the ability to withstand various stresses including antibiotics. In a clinical setting bacterial persistence often leads to the recalcitrance of various infections increasing the treatment time and costs. Additionally, some studies also indicate that persistence can also pave way for the emergence of resistant strains. In a laboratory setting this persistent phenotype is enriched in nutritionally deprived environments. Consequently, in a batch culture the late stationary phase is enriched with persistent bacteria. The mechanism of persister cell formation and its regulation is not well understood. Toxin-antitoxins (TA) systems have been implicated to be responsible for bacterial persistence and rifampicin is used to treat highly persistent bacterial strains. The current study tries to explore a possible interaction between rifampicin and the MazEF TA system that furthers the former’s success rate in treating persistent bacteria. Results: In the current study we found that the population of bacteria in the death phase of a batch culture consists of metabolically inactive live cells resembling persisters, which showed higher membrane depolarization as compared to the log phase bacteria. We also observed an increase in the expression of the MazEF TA modules in this phase. Since rifampicin is used to kill the persisters, we assessed the interaction of rifampicin with MazEF complex. We showed that rifampicin moderately interacts with MazEF complex with 1:1 stoichiometry.Conclusion: Our study suggests that the interaction of rifampicin with MazEF complex might play an important role in inhibition of persisters.

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For the greater good: Programmed cell death in bacterial communities

Cited by 76 publications

References 80 publications

Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents

Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents

Dual functionality of the TasA amyloid protein inBacillusphysiology and fitness on the phylloplane

MazEF-rifampicin interaction suggests a mechanism for rifampicin induced inhibition of persisters

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