{"id":165,"date":"2024-04-26T10:09:43","date_gmt":"2024-04-26T10:09:43","guid":{"rendered":"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/?page_id=165"},"modified":"2026-06-24T13:17:19","modified_gmt":"2026-06-24T13:17:19","slug":"key-publications","status":"publish","type":"page","link":"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/key-publications\/","title":{"rendered":"Key Publications"},"content":{"rendered":"\n<p class=\"has-text-align-center\"><a href=\"https:\/\/scholar.google.co.uk\/citations?user=jMi2d0UAAAAJ&amp;hl=en&amp;oi=ao\" data-type=\"URL\">Please click here for a full list of publications.<\/a><\/p>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><a href=\"https:\/\/journals.plos.org\/plosbiology\/article?id=10.1371\/journal.pbio.3003658\"><strong>CRISPR-Cas is beneficial in plasmid competition, but limited by competitor toxin\u2013antitoxin activity when horizontally transferred<\/strong>.<\/a> (<strong>S\u00fcnderhauf et al., PLoS Biology 2026<\/strong>)<\/p>\n\n\n\n<ul>\n<li><em>Abstract:<\/em> Bacteria can encode dozens of different immune systems that protect them from infection by mobile genetic elements (MGEs). MGEs themselves may also carry immune systems, such as CRISPR-Cas, to target competitor MGEs. It is unclear when this is favored by natural selection, and whether toxin\u2013antitoxin (TA) systems\u2014common competitive mechanisms carried by plasmids\u2014can alter their efficacy. Here, we develop and test novel theory to analyze the outcome of competition between plasmids when one carries a CRISPR-Cas system that targets the other plasmid. Our mathematical model and experiments using Escherichia coli and competing IncP plasmids reveal that plasmid-borne CRISPR-Cas is beneficial to the plasmid carrying it when the plasmid has not recently transferred to a new host. However, CRISPR-Cas is selected against when the plasmid carrying it transfers horizontally, if a resident competitor plasmid encodes a TA system that elicits post-segregational killing. Consistent with a TA barrier to plasmid-borne CRISPR-Cas, a bioinformatic analysis reveals that naturally occurring CRISPR-Cas-bearing plasmids avoid targeting other plasmids with TA systems across bacterial genera. Our work shows how the benefit of plasmid-borne CRISPR-Cas is severely reduced against TA-encoding competitor plasmids, but only when plasmid-borne CRISPR-Cas is horizontally transferred. These findings have key implications for the distribution of prokaryotic defenses and our understanding of their role in competition between MGEs, and the utility of CRISPR-Cas as a tool to remove plasmids from pathogenic bacteria.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/journals.plos.org\/plosbiology\/article?id=10.1371\/journal.pbio.3003842\">Eco-evolutionary feedbacks drive the co-occurrence of restriction-modification systems and antimicrobial resistance genes in bacteria.<\/a> (Westley et al., PLoS Biology 2026)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Abstract: <\/em>Bacterial pathogens commonly become drug resistant via horizontal acquisition of antimicrobial resistance genes (ARGs), which are often encoded on mobile genetic elements (MGEs). Although bacterial defence systems are typically considered barriers to horizontal gene transfer (HGT), previous studies revealed that bacteria with more restriction-modification (RM) systems (the most abundant bacterial defences) frequently carry more MGEs. It was suggested that this counterintuitive relationship might result from stronger selection for RM systems when exposure to costly MGEs increases. Here, we test this hypothesis using a combination of modeling and bioinformatics analysis of &gt;40,000 bacterial genomes to better understand how eco-evolutionary feedbacks between selection for RM and acquisition of MGEs shape bacterial genome evolution. Our model predicts negative associations between HGT and RM, but only if RM diversity is high. By contrast, at low RM diversity, eco-evolutionary feedbacks drive the emergence of positive associations between HGT and RM. Consistent with these predictions, we identified negative relationships between acquired ARG counts and RM counts across species but positive relationships within individual species. Collectively, our work helps to understand how RM systems shape patterns of HGT of ARGs, which may offer opportunities for targeted surveillance of strains at higher risk of horizontally acquiring novel drug resistance alleles.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/pmc.ncbi.nlm.nih.gov\/articles\/PMC12409350\/\">Phage provoke growth delays and SOS response induction despite CRISPR-Cas protection. <\/a>(Pons et al., Phil Trans B 2025)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Abstract:<\/em> Bacteria evolve resistance against their phage foes with a wide range of resistance strategies whose costs and benefits depend on the level of protection they confer and on the costs for maintainance.&nbsp;<em>Pseudomonas aeruginosa<\/em>&nbsp;can evolve resistance against its phage DMS<em>3vir<\/em>&nbsp;either by surface mutations that prevent phage binding or through CRISPR-Cas immunity. CRISPR immunity carries an inducible cost whose exact origin is still unknown, and previous work suggested it stems from the inability of the CRISPR-Cas system to completely prevent phage DNA injection and subsequent gene expression before clearing the phage infection. However, the bacterial processes involved are still unknown, and we hypothesize that CRISPR-immunity-associated costs could come from increased mortality rate or reduced growth ability compared with surface-resistant bacteria. To tease apart these two mechanisms with divergent ecological consequences, we use a novel microfluidics-based single-cell approach combined with flow cytometry methods to monitor the effects of phage exposure on the survival and growth of its host. We observed that while CRISPR immunity protects from phage-induced lysis, it cannot prevent phage-induced division lag, filamentation and SOS response activation in a subpopulation of the host bacteria. These results suggest that the costs associated with CRISPR immunity at the population level are caused by heterogeneity in phage-induced growth defects.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/doi.org\/10.1101\/2023.07.23.550022\">Antibiotics of the future are prone to resistance in Gram-negative pathogens. <\/a>(Daruka et al., 2024)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Abstract: <\/em>Despite the ongoing development of new antibiotics, the future evolution of bacterial resistance may render them ineffective. We demonstrate that antibiotic candidates currently under development are as prone to resistance evolution in Gram-negative pathogens as clinically employed antibiotics. Resistance generally stems from both genomic mutations and the transfer of antibiotic resistance genes from microbiomes associated with humans, both factors carrying equal significance. The molecular mechanisms of resistance overlap with those found in commonly used antibiotics. Therefore, these mechanisms are already present in natural populations of pathogens, indicating that resistance can rapidly emerge through selection of pre-existing bacterial variants. However, certain combinations of antibiotics and bacterial strains are less prone to developing resistance, emphasizing the potential of narrow-spectrum antibacterial therapies that could remain effective. Our comprehensive framework allows for predicting future health risks associated with bacterial resistance to new antibiotics.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/doi.org\/10.7554\/eLife.99752.1\">Heterogeneous efflux pump expression underpins phenotypic resistance to antimicrobial peptides. <\/a>(Maestri et al., Cell Host &amp; Microbe 2024)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Abstract: <\/em>Antimicrobial resistance threatens the viability of modern medical interventions. There is a dire need of developing novel approaches to counter resistance mechanisms employed by starved or slow-growing pathogens that are refractory to conventional antimicrobial therapies. Antimicrobial peptides have been advocated as potential therapeutic solutions due to low levels of genetic resistance observed in bacteria against these compounds. However, here we show that subpopulations of stationary phase&nbsp;<em>Escherichia coli<\/em>&nbsp;and&nbsp;<em>Pseudomonas aeruginosa<\/em>&nbsp;survive tachyplesin treatment without genetic mutations. These phenotypic variants induce efflux, outer membrane vesicles secretion and membrane modifications in response to tachyplesin exposure, sequestering the peptide in their membranes where it cannot exert its antimicrobial activity. We discovered that formation of these phenotypic variants could be prevented by administering tachyplesin in combination with sertraline, a clinically used antidepressant, suggesting a novel approach for combatting antimicrobial-refractory stationary phase bacteria.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/doi.org\/10.1016\/j.chom.2024.07.005\">The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape.<\/a><a href=\"https:\/\/www.sciencedirect.com\/science\/article\/pii\/S1369527424000122\"> <\/a>(Maestri et al., Cell Host &amp; Microbe 2024)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Summary: <\/em>The constant arms race between bacteria and their parasites has resulted in a large diversity of bacterial defenses, with many bacteria carrying multiple systems. Here, we report the discovery of a phylogenetically widespread defense system, coined methylation-associated defense system (MADS), which is distributed across gram-positive and gram-negative bacteria. MADS interacts with a CRISPR-Cas system in its native host to provide robust and durable resistance against phages. While phages can acquire epigenetic-mediated resistance against MADS, co-existence of MADS and a CRISPR-Cas system limits escape emergence. MADS comprises eight genes with predicted nuclease, ATPase, kinase, and methyltransferase domains, most of which are essential for either self\/non-self discrimination, DNA restriction, or both. The complex genetic architecture of MADS and MADS-like systems, relative to other prokaryotic defenses, points toward highly elaborate mechanisms of sensing infections, defense activation, and\/or interference.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/www.sciencedirect.com\/science\/article\/pii\/S1369527424000122\">Multi-layered genome defences in bacteria. <\/a>(Agapov et al., Current Opinion in Microbiology 2024)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Summary<\/em>: Bacteria have evolved a variety of defence mechanisms to protect against&nbsp;mobile genetic elements, including restriction-modification systems and CRISPR\u2013Cas. In recent years, dozens of previously unknown defence systems (DSs) have been discovered. Notably, diverse DSs often coexist within the same genome, and some co-occur at frequencies significantly higher than would be expected by chance, implying potential synergistic interactions. Recent studies have provided evidence of defence mechanisms that enhance or complement one another. Here, we review the interactions between DSs at the mechanistic, regulatory, ecological&nbsp;and evolutionary levels.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><strong><a href=\"https:\/\/www.nature.com\/articles\/d41586-023-03796-8\">Viruses wrap up bacterial defences. <\/a>(Blower and van Houte, Nature 2024)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Summary: <\/em>Bacteria use diverse defences against viral predators called bacteriophages. A method to identify antibacterial counter-defences in viral genomes has revealed striking modes of defence inhibition.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<p><a href=\"https:\/\/pubmed.ncbi.nlm.nih.gov\/38366022\/\"><strong>CRISPR-Cas in Pseudomonas aeruginosa provides transient population-level immunity against high phage exposures<\/strong>.<\/a> <strong>(Watson et al., ISME J. 2024)<\/strong><\/p>\n\n\n\n<ul>\n<li><em>Abstract: <\/em>The prokaryotic adaptive immune system, CRISPR-Cas (clustered regularly interspaced short palindromic repeats; CRISPR-associated), requires the acquisition of spacer sequences that target invading mobile genetic elements such as phages. Previous work has identified ecological variables that drive the evolution of CRISPR-based immunity of the model organism Pseudomonas aeruginosa PA14 against its phage DMS3vir, resulting in rapid phage extinction. However, it is unclear if and how stable such acquired immunity is within bacterial populations, and how this depends on the environment. Here, we examine the dynamics of CRISPR spacer acquisition and loss over a 30-day evolution experiment and identify conditions that tip the balance between long-term maintenance of immunity versus invasion of alternative resistance strategies that support phage persistence. Specifically, we find that both the initial phage dose and reinfection frequencies determine whether or not acquired CRISPR immunity is maintained in the long term, and whether or not phage can coexist with the bacteria. At the population genetics level, emergence and loss of CRISPR immunity are associated with high levels of spacer diversity that subsequently decline due to invasion of bacteria carrying pilus-associated mutations. Together, these results provide high resolution of the dynamics of CRISPR immunity acquisition and loss and demonstrate that the cumulative phage burden determines the effectiveness of CRISPR over ecologically relevant timeframes.<\/li>\n<\/ul>\n\n\n\n<div style=\"height:30px\" aria-hidden=\"true\" class=\"wp-block-spacer\"><\/div>\n\n\n\n<figure class=\"wp-block-gallery has-nested-images columns-default is-cropped wp-block-gallery-1 is-layout-flex wp-block-gallery-is-layout-flex\">\n<figure class=\"wp-block-image size-large\"><img loading=\"lazy\" decoding=\"async\" width=\"1024\" height=\"768\" data-id=\"143\" src=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0719-1024x768.jpg\" alt=\"\" class=\"wp-image-143\" srcset=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0719-1024x768.jpg 1024w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0719-300x225.jpg 300w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0719-768x576.jpg 768w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0719-1536x1152.jpg 1536w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0719.jpg 2016w\" sizes=\"(max-width: 1024px) 100vw, 1024px\" \/><\/figure>\n\n\n\n<figure class=\"wp-block-image size-large\"><img loading=\"lazy\" decoding=\"async\" width=\"1024\" height=\"768\" data-id=\"139\" src=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0717-1024x768.jpg\" alt=\"\" class=\"wp-image-139\" srcset=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0717-1024x768.jpg 1024w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0717-300x225.jpg 300w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0717-768x576.jpg 768w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0717-1536x1152.jpg 1536w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0717.jpg 2016w\" sizes=\"(max-width: 1024px) 100vw, 1024px\" \/><\/figure>\n\n\n\n<figure class=\"wp-block-image size-large\"><img loading=\"lazy\" decoding=\"async\" width=\"1024\" height=\"768\" data-id=\"137\" src=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0716-1024x768.jpg\" alt=\"\" class=\"wp-image-137\" srcset=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0716-1024x768.jpg 1024w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0716-300x225.jpg 300w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0716-768x576.jpg 768w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0716-1536x1152.jpg 1536w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0716.jpg 2016w\" sizes=\"(max-width: 1024px) 100vw, 1024px\" \/><\/figure>\n\n\n\n<figure class=\"wp-block-image size-large\"><img loading=\"lazy\" decoding=\"async\" width=\"1024\" height=\"768\" data-id=\"127\" src=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0707-1024x768.jpg\" alt=\"\" class=\"wp-image-127\" srcset=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0707-1024x768.jpg 1024w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0707-300x225.jpg 300w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0707-768x576.jpg 768w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0707-1536x1152.jpg 1536w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0707.jpg 2016w\" sizes=\"(max-width: 1024px) 100vw, 1024px\" \/><\/figure>\n\n\n\n<figure class=\"wp-block-image size-large\"><img loading=\"lazy\" decoding=\"async\" width=\"1024\" height=\"768\" data-id=\"129\" src=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0708-1024x768.jpg\" alt=\"\" class=\"wp-image-129\" srcset=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0708-1024x768.jpg 1024w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0708-300x225.jpg 300w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0708-768x576.jpg 768w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0708-1536x1152.jpg 1536w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0708.jpg 2016w\" sizes=\"(max-width: 1024px) 100vw, 1024px\" \/><\/figure>\n\n\n\n<figure class=\"wp-block-image size-large\"><img loading=\"lazy\" decoding=\"async\" width=\"1024\" height=\"768\" data-id=\"131\" src=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0711-1024x768.jpg\" alt=\"\" class=\"wp-image-131\" srcset=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0711-1024x768.jpg 1024w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0711-300x225.jpg 300w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0711-768x576.jpg 768w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0711-1536x1152.jpg 1536w, https:\/\/sites.exeter.ac.uk\/vanhoutelab\/wp-content\/uploads\/sites\/399\/2024\/04\/IMG_0711.jpg 2016w\" sizes=\"(max-width: 1024px) 100vw, 1024px\" \/><\/figure>\n<\/figure>\n","protected":false},"excerpt":{"rendered":"<p>Please click here for a full list of publications. CRISPR-Cas is beneficial in plasmid competition, but limited by competitor toxin\u2013antitoxin activity when horizontally transferred. (S\u00fcnderhauf et al., PLoS Biology 2026) Eco-evolutionary feedbacks drive the co-occurrence of restriction-modification systems and antimicrobial resistance genes in bacteria. (Westley et al., PLoS Biology 2026) Phage provoke growth delays and [&hellip;]<\/p>\n","protected":false},"author":1575,"featured_media":125,"parent":0,"menu_order":0,"comment_status":"closed","ping_status":"closed","template":"page-sidebar-boxed-feature-img.php","meta":{"_acf_changed":false,"footnotes":""},"categories":[],"tags":[],"acf":[],"yoast_head":"<!-- This site is optimized with the Yoast SEO plugin v23.0 - https:\/\/yoast.com\/wordpress\/plugins\/seo\/ -->\n<title>Key Publications - Van Houte Lab<\/title>\n<meta name=\"description\" content=\"A selection of literature published by Stineke Van Houte and colleagues, with focus on bacterial defenses and phage therapy.\" \/>\n<meta name=\"robots\" content=\"index, follow, max-snippet:-1, max-image-preview:large, max-video-preview:-1\" \/>\n<link rel=\"canonical\" href=\"https:\/\/sites.exeter.ac.uk\/vanhoutelab\/key-publications\/\" \/>\n<meta property=\"og:locale\" content=\"en_US\" \/>\n<meta property=\"og:type\" content=\"article\" \/>\n<meta property=\"og:title\" content=\"Key Publications - 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