4.5 Article

Fitness benefits to bacteria of carrying prophages and prophage-encoded antibiotic-resistance genes peak in different environments

期刊

EVOLUTION
卷 75, 期 2, 页码 515-528

出版社

OXFORD UNIV PRESS
DOI: 10.1111/evo.14153

关键词

Antibiotic resistance; fitness; lysogen; mobile genetic elements; prophage; temperate phage

资金

  1. European Union's Horizon 2020 research and innovation programme under the Marie Skodowska-Curie grant [794447-ProphARG]
  2. Swiss National Science Foundation [PZ00P3_179743]
  3. Competence Center Environment and Sustainability of the ETH [0-21248-08]
  4. Swiss National Science Foundation (SNF) [PZ00P3_179743] Funding Source: Swiss National Science Foundation (SNF)

向作者/读者索取更多资源

Research shows that the benefits of prophages and the adaptive genes they carry vary independently across different environments, affecting their role in evolution and predicting the spread of genetic elements.
Understanding the role of horizontal gene transfer (HGT) in adaptation is a key challenge in evolutionary biology. In microbes, an important mechanism of HGT is prophage acquisition (phage genomes integrated into bacterial chromosomes). Prophages can influence bacterial fitness via the transfer of beneficial genes (including antibiotic-resistance genes, ARGs), protection from superinfecting phages, or switching to a lytic lifecycle that releases free phages infectious to competitors. We expect these effects to depend on environmental conditions because of, for example, environment-dependent induction of the lytic lifecycle. However, it remains unclear how costs/benefits of prophages vary across environments. Here, studying prophages with/without ARGs in Escherichia coli, we disentangled the effects of prophages alone and adaptive genes they carry. In competition with prophage-free strains, benefits from prophages and ARGs peaked in different environments. Prophages were most beneficial when induction of the lytic lifecycle was common, whereas ARGs were more beneficial upon antibiotic exposure and with reduced prophage induction. Acquisition of prophage-encoded ARGs by competing strains was most common when prophage induction, and therefore free phages, were common. Thus, selection on prophages and adaptive genes they carry varies independently across environments, which is important for predicting the spread of mobile/integrating genetic elements and their role in evolution.

作者

我是这篇论文的作者
点击您的名字以认领此论文并将其添加到您的个人资料中。

评论

主要评分

4.5
评分不足

次要评分

新颖性
-
重要性
-
科学严谨性
-
评价这篇论文

推荐

Article Evolutionary Biology

Evolution of honey resistance in experimental populations of bacteria depends on the type of honey and has no major side effects for antibiotic susceptibility

Anna M. Bischofberger, Katia R. Pfrunder Cardozo, Michael Baumgartner, Alex R. Hall

Summary: Researchers found that bacteria increased their honey resistance by mutating genes involved in antibacterial activity of honey when adapting to different types of honey. However, they did not observe cross-resistance or collateral sensitivity against antibiotics from six different classes due to honey adaptation.

EVOLUTIONARY APPLICATIONS (2021)

Article Ecology

Human-associated microbiota suppress invading bacteria even under disruption by antibiotics

Andrew D. Letten, Michael Baumgartner, Katia R. Pfrunder-Cardozo, Jonathan M. Levine, Alex R. Hall

Summary: The competitive suppression of antibiotic-resistant strains is strongly influenced by the composition of the microbiome, with the source community playing a more significant role than antibiotic exposure. While antibiotics can disrupt community composition, the suppression of resistant strains can still be maintained despite these changes.

ISME JOURNAL (2021)

Article Ecology

Pipefish Locally Adapted to Low Salinity in the Baltic Sea Retain Phenotypic Plasticity to Cope With Ancestral Salinity Levels

Henry Goehlich, Linda Sartoris, Kim-Sara Wagner, Carolin C. Wendling, Olivia Roth

Summary: The study found that broad-nosed pipefish are locally adapted to low salinity environments, but still retain phenotypic plasticity to cope with ancestral salinity levels and prevailing pathogens.

FRONTIERS IN ECOLOGY AND EVOLUTION (2021)

Article Microbiology

Exposure to lysed bacteria can promote or inhibit growth of neighboring live bacteria depending on local abiotic conditions

Fokko Smakman, Alex R. Hall

Summary: Dead bacterial cells can either support or inhibit the growth of other bacteria based on their lysis process and the surrounding environment. Adding lysate from dead bacteria can suppress the growth of Escherichia coli, particularly affecting genes involved in motility.

FEMS MICROBIOLOGY ECOLOGY (2022)

Article Biology

Conjugative plasmid transfer is limited by prophages but can be overcome by high conjugation rates

Claudia Igler, Lukas Schwyter, Daniel Gehrig, Carolin Charlotte Wendling

Summary: This study investigates the impact of prophages on the spread of conjugative plasmids and finds that prophages can limit the spread of plasmids. The inhibitory effect is strongly influenced by environmental conditions and bacterial genetic background.

PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES (2022)

Article Microbiology

Collateral Sensitivity Interactions between Antibiotics Depend on Local Abiotic Conditions

Richard C. Allen, Katia R. Pfrunder-Cardozo, Alex R. Hall

Summary: The study found that local environmental conditions (such as pH, temperature, and bile salts) can influence collateral sensitivity of antibiotics against bacteria, potentially by promoting different sets of mutants during resistance evolution or modifying the expression of collateral effects for individual mutants.

MSYSTEMS (2021)

Article Biochemistry & Molecular Biology

Community composition of bacteria isolated from Swiss banknotes varies depending on collection environment

Anna M. Bischofberger, Alex R. Hall

Summary: Humans interact with surfaces and microbial communities in the environment. The composition of bacterial communities on banknotes varies depending on the local collection environment, but shows no evidence of geographic structure.

MOLECULAR ECOLOGY (2023)

Article Genetics & Heredity

Estimating plasmid conjugation rates: A new computational tool and a critical comparison of methods

Jana S. Huisman, Fabienne Benz, Sarah J. N. Duxbury, J. Arjan G. M. de Visser, Alex R. Hall, Egil A. J. Fischer, Sebastian Bonhoeffer

Summary: This study compares commonly used methods for measuring plasmid conjugation rates and finds that these estimates are often dependent on factors such as measurement time, population densities, and initial ratios of donor to recipient populations. The study proposes a new method to estimate conjugation rates and provides analytical expressions for the valid parameter range. In addition, a user-friendly software package and web interface are provided for accurate and comparable measurement of plasmid conjugation rates.

PLASMID (2022)

Article Genetics & Heredity

Co-transfer of functionally interdependent genes contributes to genome mosaicism in lambdoid phages

Anne Kupczok, Zachary M. Bailey, Dominik Refardt, Carolin C. Wendling

Summary: Lambdoid phages are related temperate phages that can infect gut bacteria. These phages have a mosaic genome structure and evolve by transferring genomic regions. The study identified groups of genes that are frequently co-transferred and observed that they tend to be near each other on the genome. These co-transferred genes are involved in related functions and play an important role in the evolution of the modular structure of these genomes.

MICROBIAL GENOMICS (2022)

Article Biochemistry & Molecular Biology

Suboptimal environmental conditions prolong phage epidemics in bacterial populations

Henry Goehlich, Olivia Roth, Michael Sieber, Cynthia M. Chibani, Anja Poehlein, Jelena Rajkov, Heiko Liesegang, Carolin C. Wendling

Summary: Infections by filamentous phages can influence bacterial fitness, with the production of viral particles being energetically costly. Bacteria can evolve resistance if the costs outweigh the benefits, shortening phage epidemics. The impact of abiotic conditions on host resistance evolution is still unknown.

MOLECULAR ECOLOGY (2023)

Article Microbiology

Vibrio syngnathi sp. nov., a fish pathogen, isolated from the Kiel Fjord

Cynthia Maria Chibani, Robert Hertel, Meina Neumann-Schaal, Henry Goehlich, Kim Wagner, Boyke Bunk, Cathrin Sproeer, Jorg Overmann, Michael Hoppert, Silke Mareike Marten, Olivia Roth, Heiko Liesegang, Carolin C. Wendling

Summary: A new Vibrio strain, K08M4(T), was isolated from the broad-nosed pipefish Syngnathus typhle in the Kiel Fjord. The strain showed distinct phenotypic features and its complete genome sequence was analyzed.

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY (2023)

Article Biochemistry & Molecular Biology

Prophage mediated control of higher order interactions-Insights from multi-level approaches

Carolin C. Wendling

Summary: Prophages, latent viral elements in bacterial genomes, have diverse effects on bacterial ecology and evolution. This review summarizes the latest advancements in understanding how these effects are transmitted across multiple biological systems, potentially impacting ecosystem stability and functioning. Prophages have context-specific effects on higher-order interactions, ranging from contributions to global biogeochemical processes and mutualistic interactions to negative impacts on ecosystem engineers and potential cascading effects for multiple species. Future research should adopt an integrative approach to quantify the effects of prophages in complex ecosystems.

CURRENT OPINION IN SYSTEMS BIOLOGY (2023)

Article Biology

Rapid decline of adaptation of Pseudomonas fluorescens to soil biotic environment

Pedro Gomez, Alex R. Hall, Steve Paterson, Angus Buckling

Summary: Interactions between microbes can both constrain and enhance their adaptation to the environment. In a study with a commercial potting compost microbial community, the presence of the community did not constrain the adaptation of the soil bacterium Pseudomonas fluorescens SBW25, but some mutations that were beneficial in the abiotic environment were costly in the presence of the community. Whole-genome sequencing revealed clone-specific mutations supporting multiple genetic pathways to adaptation.

BIOLOGY LETTERS (2022)

暂无数据