The landscape of lysogeny across microbial community density, diversity and energetics

Silveira, Cynthia B.; Luque, Antoni; Rohwer, Forest

doi:10.1111/1462-2920.15640

Cited by 57 publications

(55 citation statements)

References 169 publications

(327 reference statements)

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“…Lysogeny is proposed as a survival strategy for phages in oligotrophic environments ( Stewart & Levin, 1984 ), but also occurs frequently at high host densities ( Silveira, Luque & Rohwer, 2021 ). Our results show, that the lytic infection and the temperate infection PtW enabled bacterial coexistence and stable infection dynamics at low nutrient concentrations.…”

Section: Discussionmentioning

confidence: 99%

“…In our model the lysogenic infected bacteria can outcompete non-infected bacteria because of the high phage number infecting bacteria at high resource levels. In natural systems the number of phage coinfections increases at high microbial abundances, which favors phage integration and thus lysogenic infections ( Luque & Silveira, 2020 ; Silveira, Luque & Rohwer, 2021 ). A phage integration into bacterial genome at high host densities can have advantages for bacteria.…”

Section: Discussionmentioning

confidence: 99%

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Phage strategies facilitate bacterial coexistence under environmental variability

Voigt

Rall

Chatzinotas

et al. 2021

PeerJ

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Bacterial communities are often exposed to temporal variations in resource availability, which exceed bacterial generation times and thereby affect bacterial coexistence. Bacterial population dynamics are also shaped by bacteriophages, which are a main cause of bacterial mortality. Several strategies are proposed in the literature to describe infections by phages, such as “Killing the Winner”, “Piggyback the loser” (PtL) or “Piggyback the Winner” (PtW). The two temperate phage strategies PtL and PtW are defined by a change from lytic to lysogenic infection when the host density changes, from high to low or from low to high, respectively. To date, the occurrence of different phage strategies and their response to environmental variability is poorly understood. In our study, we developed a microbial trophic network model using ordinary differential equations (ODEs) and performed ‘in silico’ experiments. To model the switch from the lysogenic to the lytic cycle, we modified the lysis rate of infected bacteria and their growth was turned on or off using a density-dependent switching point. We addressed whether and how the different phage strategies facilitate bacteria coexistence competing for limiting resources. We also studied the impact of a fluctuating resource inflow to evaluate the response of the different phage strategies to environmental variability. Our results show that the viral shunt (i.e. nutrient release after bacterial lysis) leads to an enrichment of the system. This enrichment enables bacterial coexistence at lower resource concentrations. We were able to show that an established, purely lytic model leads to stable bacterial coexistence despite fluctuating resources. Both temperate phage models differ in their coexistence patterns. The model of PtW yields stable bacterial coexistence at a limited range of resource supply and is most sensitive to resource fluctuations. Interestingly, the purely lytic phage strategy and PtW both result in stable bacteria coexistence at oligotrophic conditions. The PtL model facilitates stable bacterial coexistence over a large range of stable and fluctuating resource inflow. An increase in bacterial growth rate results in a higher resilience to resource variability for the PtL and the lytic infection model. We propose that both temperate phage strategies represent different mechanisms of phages coping with environmental variability. Our study demonstrates how phage strategies can maintain bacterial coexistence in constant and fluctuating environments.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Phage strategies facilitate bacterial coexistence under environmental variability

Voigt

Rall

Chatzinotas

et al. 2021

PeerJ

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“…The internal volumes of these capsids accommodate genomes spanning three orders of magnitude in length, from 5 kilobase pairs (kbp) to 735 kbp [82] , [62] . The diversity in genome length and genomic content of tailed phages may explain their key role in regulating ecosystems [86] , [113] , in promoting the evolution of microbes [129] , [67] , [121] , in participating strongly in the planetary carbon cycle [74] , and in becoming the most abundant biological entity on the planet [27] . However, the role of the diversity in tailed phage capsid architectures and genome lengths across ecosystems remains unclear.…”

Section: Introductionmentioning

confidence: 99%

Predicting the capsid architecture of phages from metagenomic data

Lee

Bartels

McNair

et al. 2022

Computational and Structural Biotechnology Journal

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“…Co-adaptation has also been observed with CrAss-like-phages (e.g., FCrAss001) that co-exist with their Bacteroides host and persist in high abundance in the human gut [15] through a lytic-lysogeny intermediate [14, 16]. Dense populations of replicating bacteria [17, 18], as found in the gut, show increased rates of lysogeny through ‘piggyback-the-winner’ dynamics [19, 20]. Increased bacterial density increases the rate of lysogeny by phage coinfection [20], or through host-density regulated molecular switches [21].…”

Section: Introductionmentioning

confidence: 99%

“…Once integrated, prophages can provide a fitness advantage to their bacterial host through protection from further infection by superinfection exclusion or immunity [22], and the introduction of new genes encoding for virulence factors, antibiotic resistance, or novel metabolic functions [23]. In this case, prophages persist by 'making-the-winner' [20].…”

Section: Introductionmentioning

confidence: 99%

Bacteriophages Playing Nice: Lysogenic bacteriophage replication stable in the human gut microbiota

Sutcliffe

Reyes²,

Maurice

2022

Preprint

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The human gut is a dense microbial community, of which bacteria and bacteriophages are the majority. Bacteriophages, viruses of bacteria, exist stably, without major fluctuations in the gut of healthy individuals. This stability appears to be due to an absence of "kill-the-winner" dynamics, and the existence of "piggy- back-the-winner" dynamics, where lysogenic replication rather than lytic replication occurs. Revisiting the deep-viral sequencing data of a healthy individual studied over 2.4 years, we were able to improve our understanding of how these dynamics occur in healthy individuals. We assembled prophages from bacterial metagenomic data and show that these prophages were continually switching from lysogenic to lytic replication. Prophages were the source of a stable extracellular phage population continually present in low abundance, in comparison to the lytic- phage population, where taxonomic diversity diverged over 2.4 years. The switch to lytic replication, or prophage induction, appears to occur mostly through spontaneous prophage induction. The observed phage dynamics of regular spontaneous induction are ecologically important as they allow prophages to maintain their ability to replicate, avoiding degradation and their loss from the gut microbiota.

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The landscape of lysogeny across microbial community density, diversity and energetics

Abstract: This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 57 publications

References 169 publications

Phage strategies facilitate bacterial coexistence under environmental variability

Phage strategies facilitate bacterial coexistence under environmental variability

Predicting the capsid architecture of phages from metagenomic data

Bacteriophages Playing Nice: Lysogenic bacteriophage replication stable in the human gut microbiota

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