Journal articles
Vos M, Wielgoss, Didelot, Velicer, Chaudhuri, Weedall, Liu (In Press). A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus.
The ISME Journal: multidisciplinary journal of microbial ecologyAbstract:
A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus
The bacterium Myxococcus xanthus glides through soil in search of prey microbes, but when food sources run out, cells cooperatively construct and sporulate within multicellular fruiting bodies. M. xanthus strains isolated from a 16x16 centimetre-scale patch of soil were previously shown to have diversified into many distinct compatibility types that are distinguished by the failure of swarming colonies to merge upon encounter. We sequenced the genomes of 22 isolates from this population belonging to the two most frequently occurring MultiLocus Sequence Type (MLST) clades in order to trace patterns of incipient genomic divergence, specifically related to social divergence. Although homologous recombination occurs frequently within the two MLST clades, we find an almost complete absence of recombination events between them. As the two clades are very closely related and live in sympatry, either ecological or genetic barriers must reduce genetic exchange between them. We find that the rate of change in the accessory genome is greater than the rate of amino acid substitution in the core genome. We identify a large genomic tract that consistently differs between isolates that do not freely merge and therefore is a candidate region for harbouring gene(s) responsible for self/non-self discrimination.
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Lear L, Padfield D, Hesse E, Kay S, Buckling A, Vos M (In Press). Copper Reduces the Virulence of Bacterial Communities at Environmentally Relevant Concentrations.
Lear L, Hesse E, Buckling A, Vos M (In Press). Copper Selects for Siderophore-Mediated Virulence in Pseudomonas Aeruginosa.
Vos M, Andreani NA (In Press). Prokaryote genome fluidity is dependent on effective population size. ISME Journal
White H, Sheppard S, Raymond B, Vos M, Pascoe B (In Press). Signatures of selection in core and accessory genomes indicate different. ecological drivers of diversification among Bacillus cereus clades.
Molecular EcologyAbstract:
Signatures of selection in core and accessory genomes indicate different. ecological drivers of diversification among Bacillus cereus clades
Bacterial clades are often ecologically distinct, despite extensive horizontal gene transfer (HGT). How selection works on different parts of bacterial pan-genomes to drive and maintain the emergence of clades is unclear. Focussing on the three largest clades in the diverse and well-studied Bacillus cereus sensu lato group, we identified clade-specific core genes (present in all clade members) and then used clade-specific allelic diversity to identify genes under purifying and diversifying selection. Clade-specific accessory genes (present in a subset of strains within a clade) were characterized as being under selection using presence/absence in specific clades. Gene ontology analyses of genes under selection revealed that different core genes and gene functions were enriched in different clades. Furthermore, some gene functions were enriched only amongst clade-specific core or accessory genomes. Genes under purifying selection were often clade-specific, while genes under diversifying selection showed signs of frequent HGT. These patterns are consistent with different selection pressures acting on both the core and accessory genomes of different clades and can lead to ecological divergence in both cases. Examining variation in allelic diversity allows us to uncover genes under clade-specific selection, allowing ready identification of strains and their ecological niche.
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Vos M (2023). Accessory microbiomes.
Microbiology (Reading),
169(5).
Abstract:
Accessory microbiomes.
In microbiome research, considerable effort has been invested in finding core microbiomes, which have been hypothesized to contain the species most important for host function. Much less attention has been paid to microbiome members that are present in only a subset of hosts. Such accessory microbiomes must in large part consist of species that have no effect on fitness, but some will have deleterious effects on fitness (pathogens), and it is also possible that some accessory microbiome members benefit an ecologically distinct subset of hosts. This short paper discusses what we know about accessory microbiomes, specifically by comparing it with the concept of accessory genomes.
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Vos M, Padfield D, Quince C, Vos R (2023). Adaptive radiations in natural populations of prokaryotes: innovation is key.
FEMS Microbiol EcolAbstract:
Adaptive radiations in natural populations of prokaryotes: innovation is key.
Prokaryote diversity makes up most of the tree of life and is crucial to the functioning of the biosphere and human health. However, the patterns and mechanisms of prokaryote diversification have received relatively little attention compared to animals and plants. Adaptive radiation, the rapid diversification of an ancestor species into multiple ecologically divergent species, is a fundamental process by which macrobiological diversity is generated. Here, we discuss whether ecological opportunity could lead to similar bursts of diversification in bacteria. We explore how adaptive radiations in prokaryotes can be kickstarted by horizontally acquired key innovations allowing lineages to invade new niche space that subsequently is partitioned among diversifying specialist descendants. We discuss how novel adaptive zones are colonised and exploited after the evolution of a key innovation and whether certain types of are more prone to adaptive radiation. Radiation into niche specialists does not necessarily lead to speciation in bacteria when barriers to recombination are absent. We propose that in this scenario, niche-specific genes could accumulate within a single lineage, leading to the evolution of an open pan-genome.
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Winter M, Harms K, Johnsen P, Vos M (2023). Collection of Annotated Acinetobacter Genome Sequences.
Microbiol Resour Announc,
12(3).
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Collection of Annotated Acinetobacter Genome Sequences.
The genus Acinetobacter contains environmental species as well as opportunistic pathogens of humans. Several species are competent for natural transformation, an important mechanism of horizontal gene transfer. Here, we present the genome sequences of 19 Acinetobacter strains used in past and upcoming studies of natural transformation.
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Winter M, Harms K, Johnsen PJ, Buckling A, Vos M (2023). Testing for the fitness benefits of natural transformation during community-embedded evolution.
Microbiology (Reading),
169(8).
Abstract:
Testing for the fitness benefits of natural transformation during community-embedded evolution.
Natural transformation is a process where bacteria actively take up DNA from the environment and recombine it into their genome or reconvert it into extra-chromosomal genetic elements. The evolutionary benefits of transformation are still under debate. One main explanation is that foreign allele and gene uptake facilitates natural selection by increasing genetic variation, analogous to meiotic sex. However, previous experimental evolution studies comparing fitness gains of evolved transforming- and isogenic non-transforming strains have yielded mixed support for the 'sex hypothesis.' Previous studies testing the sex hypothesis for natural transformation have largely ignored species interactions, which theory predicts provide conditions favourable to sex. To test for the adaptive benefits of bacterial transformation, the naturally transformable wild-type Acinetobacter baylyi and a transformation-deficient ∆comA mutant were evolved for 5 weeks. To provide strong and potentially fluctuating selection, A. baylyi was embedded in a community of five other bacterial species. DNA from a pool of different Acinetobacter strains was provided as a substrate for transformation. No effect of transformation ability on the fitness of evolved populations was found, with fitness increasing non-significantly in most treatments. Populations showed fitness improvement in their respective environments, with no apparent costs of adaptation to competing species. Despite the absence of fitness effects of transformation, wild-type populations evolved variable transformation frequencies that were slightly greater than their ancestor which potentially could be caused by genetic drift.
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Lear L, Hesse E, Newsome L, Gaze W, Buckling A, Vos M (2023). The effect of metal remediation on the virulence and antimicrobial resistance of the opportunistic pathogen <i>Pseudomonas aeruginosa</i>.
Evolutionary Applications,
16(7), 1377-1389.
Abstract:
The effect of metal remediation on the virulence and antimicrobial resistance of the opportunistic pathogen Pseudomonas aeruginosa
AbstractAnthropogenic metal pollution can result in co‐selection for antibiotic resistance and potentially select for increased virulence in bacterial pathogens. Metal‐polluted environments can select for the increased production of siderophore molecules to detoxify non‐ferrous metals. However, these same molecules also aid the uptake of ferric iron, a limiting factor for within‐host pathogen growth, and are consequently a virulence factor. Anthropogenic methods to remediate environmental metal contamination commonly involve amendment with lime‐containing materials. However, whether this reduces in situ co‐selection for antibiotic resistance and siderophore‐mediated virulence remains unknown. Here, using microcosms containing non‐sterile metal‐contaminated river water and sediment, we test whether liming reduces co‐selection for these pathogenicity traits in the opportunistic pathogen Pseudomonas aeruginosa. To account for the effect of environmental structure, which is known to impact siderophore production, microcosms were incubated under either static or shaking conditions. Evolved P. aeruginosa populations had greater fitness in the presence of toxic concentrations of copper than the ancestral strain and showed increased resistance to the clinically relevant antibiotics apramycin, cefotaxime and trimethoprim, regardless of lime addition or environmental structure. Although we found virulence to be significantly associated with siderophore production, neither virulence nor siderophore production significantly differed between the four treatments. Furthermore, liming did not mitigate metal‐imposed selection for antibiotic resistance or virulence in P. aeruginosa. Consequently, metal‐contaminated environments may select for antibiotic resistance and virulence traits even when treated with lime.
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Bartlett A, Padfield D, Lear L, Bendall R, Vos M (2022). A comprehensive list of bacterial pathogens infecting humans. Microbiology, 168(12).
Soni V, Vos M, Eyre-Walker A (2022). A new test suggests hundreds of amino acid polymorphisms in humans are subject to balancing selection.
PLoS Biol,
20(6).
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A new test suggests hundreds of amino acid polymorphisms in humans are subject to balancing selection.
The role that balancing selection plays in the maintenance of genetic diversity remains unresolved. Here, we introduce a new test, based on the McDonald-Kreitman test, in which the number of polymorphisms that are shared between populations is contrasted to those that are private at selected and neutral sites. We show that this simple test is robust to a variety of demographic changes, and that it can also give a direct estimate of the number of shared polymorphisms that are directly maintained by balancing selection. We apply our method to population genomic data from humans and provide some evidence that hundreds of nonsynonymous polymorphisms are subject to balancing selection.
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Lear L, Padfield D, Dowsett T, Jones M, Kay S, Hayward A, Vos M (2022). Bacterial colonisation dynamics of household plastics in a coastal environment.
Sci Total Environ,
838(Pt 4).
Abstract:
Bacterial colonisation dynamics of household plastics in a coastal environment.
Accumulation of plastics in the marine environment has widespread detrimental consequences for ecosystems and wildlife. Marine plastics are rapidly colonised by a wide diversity of bacteria, including human pathogens, posing potential risks to health. Here, we investigate the effect of polymer type, residence time and estuarine location on bacterial colonisation of common household plastics, including pathogenic bacteria. We submerged five main household plastic types: low-density PE (LDPE), high-density PE (HDPE), polypropylene (PP), polyvinyl chloride (PVC) and polyethylene terephthalate (PET) at an estuarine site in Cornwall (U.K.) and tracked bacterial colonisation dynamics. Using both culture-dependent and culture-independent approaches, we found that bacteria rapidly colonised plastics irrespective of polymer type, reaching culturable densities of up to 1000 cells cm3 after 7 weeks. Community composition of the biofilms changed over time, but not among polymer types. The presence of pathogenic bacteria, quantified using the insect model Galleria mellonella, increased dramatically over a five-week period, with Galleria mortality increasing from 4% in week one to 65% in week five. No consistent differences in virulence were observed between polymer types. Pathogens isolated from plastic biofilms using Galleria enrichment included Serratia and Enterococcus species and they harboured a wide range of antimicrobial resistance genes. Our findings show that plastics in coastal waters are rapidly colonised by a wide diversity of bacteria independent of polymer type. Further, our results show that marine plastic biofilms become increasingly associated with virulent bacteria over time.
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Choufa C, Tidjani A-R, Gauthier A, Harb M, Lao J, Leblond-Bourget N, Vos M, Leblond P, Bontemps C (2022). Prevalence and mobility of integrative and conjugative elements within a Streptomyces natural population. Frontiers in Microbiology, 13
Winter M, Buckling A, Harms K, Johnsen PJ, Vos M (2021). Antimicrobial resistance acquisition via natural transformation: context is everything.
Curr Opin Microbiol,
64, 133-138.
Abstract:
Antimicrobial resistance acquisition via natural transformation: context is everything.
Natural transformation is a process where bacterial cells actively take up free DNA from the environment and recombine it into their genome or reconvert it into extra-chromosomal genetic elements. Although this mechanism is known to mediate the uptake of antibiotic resistance determinants in a range of human pathogens, its importance in the spread of antimicrobial resistance is not always appreciated. This review highlights the context in which transformation takes place: in diverse microbiomes, in interaction with other forms of horizontal gene transfer and in increasingly polluted environments. This examination of the abiotic and biotic drivers of transformation reveals that it could be more important in the dissemination of resistance genes than is often recognised.
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Lear L, Hesse E, Buckling A, Vos M (2021). Copper selects for siderophore-mediated virulence in <i>Pseudomonas aeruginosa</i>.
Abstract:
Copper selects for siderophore-mediated virulence in Pseudomonas aeruginosa
AbstractIron is essential for almost all bacterial pathogens and consequently it is actively withheld by their hosts. However, the production of extracellular siderophores enables iron sequestration by pathogens, increasing their virulence. Another function of siderophores is extracellular detoxification of non-ferrous metals. Here, we experimentally link the detoxification and virulence roles of siderophores by testing whether the opportunistic pathogen Pseudomonas aeruginosa displays greater virulence after exposure to copper. To do this, we incubated P. aeruginosa under different environmentally relevant copper regimes for either two or twelve days. Subsequent growth in a copper-free environment removed phenotypic effects, before we quantified pyoverdine production (the primary siderophore produced by P. aeruginosa), and virulence using the Galleria mellonella infection model. Copper selected for increased pyoverdine production, which was positively correlated with virulence. This effect increased with time, such that populations incubated with high copper for twelve days were the most virulent. Replication of the experiment with a non-pyoverdine producing strain of P. aeruginosa demonstrated that pyoverdine production was largely responsible for the change in virulence. Therefore we here show a direct link between metal stress and bacterial virulence, highlighting another dimension of the detrimental effects of metal pollution on human health.
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Stefanic P, Belcijan K, Kraigher B, Kostanjšek R, Nesme J, Madsen JS, Kovac J, Sørensen SJ, Vos M, Mandic-Mulec I, et al (2021). Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis.
Nat Commun,
12(1).
Abstract:
Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis.
Bacillus subtilis is a soil bacterium that is competent for natural transformation. Genetically distinct B. subtilis swarms form a boundary upon encounter, resulting in killing of one of the strains. This process is mediated by a fast-evolving kin discrimination (KD) system consisting of cellular attack and defence mechanisms. Here, we show that these swarm antagonisms promote transformation-mediated horizontal gene transfer between strains of low relatedness. Gene transfer between interacting non-kin strains is largely unidirectional, from killed cells of the donor strain to surviving cells of the recipient strain. It is associated with activation of a stress response mediated by sigma factor SigW in the donor cells, and induction of competence in the recipient strain. More closely related strains, which in theory would experience more efficient recombination due to increased sequence homology, do not upregulate transformation upon encounter. This result indicates that social interactions can override mechanistic barriers to horizontal gene transfer. We hypothesize that KD-mediated competence in response to the encounter of distinct neighbouring strains could maximize the probability of efficient incorporation of novel alleles and genes that have proved to function in a genomically and ecologically similar context.
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Vos M (2021). Myxococcus xanthus.
Trends Microbiol,
29(6), 562-563.
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Ferraresso J, Lawton B, Bayliss S, Sheppard S, Cardazzo B, Gaze W, Buckling A, Vos M (2020). Determining the prevalence, identity and possible origin of bacterial pathogens in soil.
Environ Microbiol,
22(12), 5327-5340.
Abstract:
Determining the prevalence, identity and possible origin of bacterial pathogens in soil.
Soil biomes are vast, exceptionally diverse and crucial to the health of ecosystems and societies. Soils also contain an appreciable, but understudied, diversity of opportunistic human pathogens. With climate change and other forms of environmental degradation potentially increasing exposure risks to soilborne pathogens, it is necessary to gain a better understanding of their ecological drivers. Here we use the Galleria mellonella insect virulence model to selectively isolate pathogenic bacteria from soils in Cornwall (UK). We find a high prevalence of pathogenic soil bacteria with two genera, Providencia and Serratia, being especially common. Providencia alcalifaciens, P. rustigianii, Serratia liquefaciens and S. plymuthica strains were studied in more detail using phenotypic virulence and antibiotic resistance assays and whole-genome sequencing. Both genera displayed low levels of antibiotic resistance and antibiotic resistance gene carriage. However, Serratia isolates were found to carry the recently characterized metallo-β-lactamase blaSPR-1 that, although not conferring high levels of resistance in these strains, poses a potential risk of horizontal transfer to other pathogens where it could be fully functional. The Galleria assay can be a useful approach to uncover the distribution and identity of pathogenic bacteria in the environment, as well as uncover resistance genes with an environmental origin.
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Madi N, Vos M, Murall CL, Legendre P, Shapiro BJ (2020). Does diversity beget diversity in microbiomes?.
Elife,
9Abstract:
Does diversity beget diversity in microbiomes?
Microbes are embedded in complex communities where they engage in a wide array of intra- and inter-specific interactions. The extent to which these interactions drive or impede microbiome diversity is not well understood. Historically, two contrasting hypotheses have been suggested to explain how species interactions could influence diversity. 'Ecological Controls' (EC) predicts a negative relationship, where the evolution or migration of novel types is constrained as niches become filled. In contrast, 'Diversity Begets Diversity' (DBD) predicts a positive relationship, with existing diversity promoting the accumulation of further diversity via niche construction and other interactions. Using high-throughput amplicon sequencing data from the Earth Microbiome Project, we provide evidence that DBD is strongest in low-diversity biomes, but weaker in more diverse biomes, consistent with biotic interactions initially favouring the accumulation of diversity (as predicted by DBD). However, as niches become increasingly filled, diversity hits a plateau (as predicted by EC).
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Vos M (2020). The evolution of bacterial pathogens in the Anthropocene. Infection, Genetics and Evolution, 86, 104611-104611.
Vos M, Sibleyras L, Lo LK, Hesse E, Gaze W, Klümper U (2020). Zinc can counteract selection for ciprofloxacin resistance.
FEMS Microbiol Lett,
367(3).
Abstract:
Zinc can counteract selection for ciprofloxacin resistance.
Antimicrobial resistance (AMR) has emerged as one of the most pressing threats to public health. AMR evolution occurs in the clinic but also in the environment, where antibiotics and heavy metals can select and co-select for AMR. While the selective potential of both antibiotics and metals is increasingly well-characterized, experimental studies exploring their combined effects on AMR evolution are rare. It has previously been demonstrated that fluoroquinolone antibiotics such as ciprofloxacin can chelate metal ions. To investigate how ciprofloxacin resistance is affected by the presence of metals, we quantified selection dynamics between a ciprofloxacin-susceptible and a ciprofloxacin-resistant Escherichia coli strain across a gradient of ciprofloxacin concentrations in presence and absence of zinc. The presence of zinc reduced growth of both strains, while ciprofloxacin inhibited exclusively the susceptible one. When present in combination zinc retained its inhibitory effect, while ciprofloxacin inhibition of the susceptible strain was reduced. Consequently, the minimal selective concentration for ciprofloxacin resistance increased up to five-fold in the presence of zinc. Environmental pollution usually comprises complex mixtures of antimicrobial agents. In addition to the usual focus on additive or synergistic interactions in complex selective mixtures, our findings highlight the importance of antagonistic selective interactions when considering resistance evolution.
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Dickinson AW, Power A, Hansen MG, Brandt KK, Piliposian G, Appleby P, O'Neill PA, Jones RT, Sierocinski P, Koskella B, et al (2019). Heavy metal pollution and co-selection for antibiotic resistance: a microbial palaeontology approach.
Environment International,
132Abstract:
Heavy metal pollution and co-selection for antibiotic resistance: a microbial palaeontology approach
Frequent and persistent heavy metal pollution has profound effects on the composition and activity of microbial communities. Heavy metals select for metal resistance but can also co-select for resistance to antibiotics, which is a global health concern. We here document metal concentration, metal resistance and antibiotic resistance along a sediment archive from a pond in the North West of the United Kingdom covering over a century of anthropogenic pollution. We specifically focus on zinc, as it is a ubiquitous and toxic metal contaminant known to co-select for antibiotic resistance, to assess the impact of temporal variation in heavy metal pollution on microbial community diversity and to quantify the selection effects of differential heavy metal exposure on antibiotic resistance. Zinc concentration and bioavailability was found to vary over the core, likely reflecting increased industrialisation around the middle of the 20th century. Zinc concentration had a significant effect on bacterial community composition, as revealed by a positive correlation between the level of zinc tolerance in culturable bacteria and zinc concentration. The proportion of zinc resistant isolates was also positively correlated with resistance to three clinically relevant antibiotics (oxacillin, cefotaxime and trimethoprim). The abundance of the class 1 integron-integrase gene, intI1, marker for anthropogenic pollutants correlated with the prevalence of zinc- and cefotaxime resistance but not with oxacillin and trimethoprim resistance. Our microbial palaeontology approach reveals that metal-contaminated sediments from depths that pre-date the use of antibiotics were enriched in antibiotic resistant bacteria, demonstrating the pervasive effects of metal-antibiotic co-selection in the environment.
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Vos M, colclough A, Corander J, Sheppard S, Bayliss S (2019). Patterns of cross‐resistance and collateral sensitivity between clinical antibiotics and natural antimicrobials. Evolutionary Applications
Vos M, Buckling A, Kuijper B (2019). Sexual Selection in Bacteria?.
Trends Microbiol,
27(12), 972-981.
Abstract:
Sexual Selection in Bacteria?
A main mechanism of lateral gene transfer in bacteria is transformation, where cells take up free DNA from the environment which subsequently can be recombined into the genome. Bacteria are also known to actively release DNA into the environment through secretion or lysis, which could aid uptake via transformation. Various evolutionary benefits of DNA uptake and DNA release have been proposed but these have all been framed in the context of natural selection. Here, we interpret bacterial DNA uptake and release in the context of sexual selection theory, which has been central to our understanding of the bewildering diversity of traits associated with sexual reproduction in the eukaryote world but has never been applied to prokaryotes. Specifically, we explore potential scenarios where bacteria releasing DNA into the environment could compete for successful uptake by other cells, or where bacteria could selectively take up DNA to enhance their fitness. We conclude that there is potential for sexual selection to act in bacteria, and that this might in part explain the considerable diversity in transformation-related behaviours.
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Andreani NA, Carraro L, Zhang L, Vos M, Cardazzo B (2019). Transposon mutagenesis in Pseudomonas fluorescens reveals genes involved in blue pigment production and antioxidant protection.
Food Microbiology,
82, 497-503.
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Transposon mutagenesis in Pseudomonas fluorescens reveals genes involved in blue pigment production and antioxidant protection.
Pseudomonas fluorescens Ps_77 is a blue-pigmenting strain able to cause food product discoloration, causing relevant economic losses especially in the dairy industry. Unlike non-pigmenting P. fluorescens, blue pigmenting strains previously were shown to carry a genomic region that includes homologs of trpABCDF genes, pointing at a possible role of the tryptophan biosynthetic pathway in production of the pigment. Here, we employ random mutagenesis to first identify the genes involved in blue-pigment production in P. fluorescens Ps_77 and second to investigate the biological function of the blue pigment. Genetic analyses based on the mapping of the random insertions allowed the identification of eight genes involved in pigment production, including the second copy of trpB (trpB_1) gene. Phenotypic characterization of Ps_77 white mutants demonstrated that the blue pigment increases oxidative-stress resistance. Indeed, while Ps_77 was growing at a normal rate in presence of 5 mM of H 2 O 2 , white mutants were completely inhibited. The antioxidative protection is not available for non-producing bacteria in co-culture with Ps_77.
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Clarke A, Azulai D, Elias Dueker M, Vos M, Perron GG (2019). Triclosan alters microbial communities in freshwater microcosms.
Water (Switzerland),
11(5).
Abstract:
Triclosan alters microbial communities in freshwater microcosms
The effect of triclosan on microbial communities that are found in soil and sediments is well documented. However, little is known regarding the possible effects of triclosan on microbial communities that are present in the column of freshwater streams as the antimicrobial is released from sediments or from water sewage outflow. We show that a concentration of triclosan as low as 1 ng/L decreases richness and evenness in freshwater microbial communities growing in the water column while using controlled experimental microcosms. Crucially, the decrease in evenness that was observed in the microbial communities was due to the selection of bacteria commonly associated with human activity, such as Acinetobacter, Pseudomonas, and Rhodobacter, as opposed to an increase in Cyanobacteria, as previously suggested. Finally, our results demonstrate that higher concentrations of triclosan comparable to heavily polluted environments can also impact the overall phylogenetic structure and community composition of microbial communities. Understanding the impact of triclosan on these microbial populations is crucial from a public health perspective as human populations are more often exposed to microbial communities that are present in the water column via recreative use.
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Hernandez RJ, Hesse E, Dowling AJ, Coyle NM, Feil EJ, Gaze WH, Vos M (2019). Using the wax moth larva Galleria mellonella infection model to detect emerging bacterial pathogens. PeerJ, 6
Vos M, Sibleyras L, Lo LK, Hesse E, Gaze W, Klümper U (2019). Zinc can counteract selection for ciprofloxacin resistance.
Abstract:
Zinc can counteract selection for ciprofloxacin resistance
AbstractAntimicrobial resistance (AMR) has emerged as one of the most pressing global threats to public health. AMR evolution occurs in the clinic but also in the environment, where low concentrations of antibiotics and heavy metals can respectively select and co-select for resistance. While the selective potential for AMR of both antibiotics and metals is increasingly well-characterized, studies exploring the combined effect of both types of selective agents are rare. It has previously been demonstrated that fluoroquinolone antibiotics such as ciprofloxacin can chelate metal ions. To investigate how ciprofloxacin resistance is affected by the presence of metals, we quantified selection dynamics between a ciprofloxacin-susceptible and an isogenic ciprofloxacin-resistantEscherichia coliMG1655 strain across a gradient of ciprofloxacin concentrations in the presence and absence of Zinc cations (Zn2+). The minimal selective concentration (MSC) for ciprofloxacin resistance significantly increased up to 5-fold in the presence of Zn2+. No such effect on the MSC was found for gentamicin, an antibiotic not known to chelate zinc cations. Environmental pollution usually consists of complex mixtures of antimicrobial agents. Our findings highlight the importance of taking antagonistic as well as additive or synergistic interactions between different chemical compounds into account when considering their effect on bacterial resistance evolution.Graphical abstractOne sentence summaryThe minimal selective concentration for a ciprofloxacin resistantE. colistrain increases up to 5-fold in the presence of Zinc cations.
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Zhang L (2018). Staphylococcus cornubiensis sp. nov. a member of the Staphylococcus intermedius Group (SIG). International Journal of Systematic and Evolutionary Microbiology
Vos M, Eyre-Walker A (2017). Are pangenomes adaptive or not?.
Nat Microbiol,
2(12).
Author URL.
Vos M, Mcleman, Buckling, Hesse, Sierocinski, Johnsen PJ, Perron GG, Huelter N (2016). No effect of natural transformation on the evolution of resistance to bacteriophages in the Acinetobacter baylyi model system. Scientific Reports
Tyc O, Song C, Dickschat JS, Vos M, Garbeva P (2016). The Ecological Role of Volatile and Soluble Secondary Metabolites Produced by Soil Bacteria.
Trends in Microbiology,
25(4), 280-292.
Abstract:
The Ecological Role of Volatile and Soluble Secondary Metabolites Produced by Soil Bacteria
© 2016 Elsevier Ltd the rich diversity of secondary metabolites produced by soil bacteria has been appreciated for over a century, and advances in chemical analysis and genome sequencing continue to greatly advance our understanding of this biochemical complexity. However, we are just at the beginning of understanding the physicochemical properties of bacterial metabolites, the factors that govern their production and ecological roles. Interspecific interactions and competitor sensing are among the main biotic factors affecting the production of bacterial secondary metabolites. Many soil bacteria produce both volatile and soluble compounds. In contrast to soluble compounds, volatile organic compounds can diffuse easily through air- and gas-filled pores in the soil and likely play an important role in long-distance microbial interactions. In this review we provide an overview of the most important soluble and volatile classes of secondary metabolites produced by soil bacteria, their ecological roles, and their possible synergistic effects.
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Koskella B, Vos M (2015). Adaptation in Natural Microbial Populations.
Annual Review of Ecology, Evolution, and Systematics,
46, 503-522.
Abstract:
Adaptation in Natural Microbial Populations
Although their diversity greatly exceeds that of plants and animals, microbial organisms have historically received less attention in ecology and evolutionary biology research. This knowledge gap is rapidly closing, owing to recent technological advances and an increasing appreciation for the role microbes play in shaping ecosystems and human health. In this review, we examine when and how the process and patterns of bacterial adaptation might fundamentally differ from those of macrobes, highlight methods used to measure adaptation in natural microbial populations, and discuss the importance of examining bacterial adaptation across multiple scales. We emphasize the need to consider the scales of adaptation as continua, in which the genetic makeup of bacteria blur boundaries between populations, species, and communities and with them concepts of ecological and evolutionary time. Finally, we examine current directions of the field as we move beyond the stamp-collecting phase and toward a better understanding of microbial adaptation in nature.
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Lee J, Murray A, Bendall R, Gaze W, Zhang L, Vos M (2015). Improved detection of Staphylococcus intermedius group in a routine diagnostic laboratory.
J Clin Microbiol,
53(3), 961-963.
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Improved detection of Staphylococcus intermedius group in a routine diagnostic laboratory.
The Staphylococcus intermedius group (SIG) includes zoonotic pathogens traditionally associated with dog bites. We describe a simple scheme for improved detection of SIG using routine laboratory methods, report its effect on isolation rates, and use sequencing to confirm that, apart from one atypical SIG strain, most isolates are Staphylococcus pseudintermedius.
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Vos M, Hesselman MC, Te Beek TA, van Passel MWJ, Eyre-Walker A (2015). Rates of Lateral Gene Transfer in Prokaryotes: High but Why?.
Trends Microbiol,
23(10), 598-605.
Abstract:
Rates of Lateral Gene Transfer in Prokaryotes: High but Why?
Lateral gene transfer is of fundamental importance to the evolution of prokaryote genomes and has important practical consequences, as evidenced by the rapid dissemination of antibiotic resistance and virulence determinants. Relatively little effort has so far been devoted to explicitly quantifying the rate at which accessory genes are taken up and lost, but it is possible that the combined rate of lateral gene transfer and gene loss is higher than that of point mutation. What evolutionary forces underlie the rate of lateral gene transfer are not well understood. We here use theory developed to explain the evolution of mutation rates to address this question and explore its consequences for the study of prokaryote evolution.
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Balážová T, Šedo O, Štefanic̈ P, Mandic̈-Mulec I, Vos M, Zdráhal Z (2014). Improvement in Staphylococcus and Bacillus strain differentiation by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry profiling by using microwave-assisted enzymatic digestion.
Rapid Communications in Mass Spectrometry,
28(17), 1855-1861.
Abstract:
Improvement in Staphylococcus and Bacillus strain differentiation by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry profiling by using microwave-assisted enzymatic digestion
RATIONALE Distinguishing between individual bacterial strains below the species level is a challenge to matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) bacterial profiling. We propose a quick method for improving strain differentiation of two Staphylococcus and one Bacillus species. METHODS an alternative procedure to the extraction protocol recommended by Bruker Daltonics was developed. Ethanol-sterilized cells of six S. aureus and six S. haemolyticus strains were digested by trypsin using 2-min microwave irradiation and were then analyzed. Twenty-eight strains belonging to two ecotypes of B. subtilis were subjected to the same procedure to extend the scope of the method. RESULTS S. aureus and S. haemolyticus strains, only partially distinguishable by the standard sample preparation procedure, were subjected to microwave-assisted tryptic digestion. The repeatability of the procedure was checked in three experiments accomplished at weekly intervals. Clear distinction of the strains was achieved by cluster analysis. The differentiation of B. subtilis ecotypes was also improved significantly by the digestion method. The discriminatory power of the novel method was supported by an increase in the number of strain-specific peaks, as compared to the standard method. CONCLUSIONS the method modulates the discriminatory power of MALDI-TOF MS profiling. The differentiation of a set of S. aureus, S. haemolyticus and B. subtilis strains was improved significantly after microwave-accelerated tryptic digestion of the cellular material. Copyright © 2014 John Wiley & Sons, Ltd.
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Wolf AB, Vos M, de Boer W, Kowalchuk GA (2013). Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria.
PLoS One,
8(12).
Abstract:
Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria.
The filamentous growth form is an important strategy for soil microbes to bridge air-filled pores in unsaturated soils. In particular, fungi perform better than bacteria in soils during drought, a property that has been ascribed to the hyphal growth form of fungi. However, it is unknown if, and to what extent, filamentous bacteria may also display similar advantages over non-filamentous bacteria in soils with low hydraulic connectivity. In addition to allowing for microbial interactions and competition across connected micro-sites, water films also facilitate the motility of non-filamentous bacteria. To examine these issues, we constructed and characterized a series of quartz sand microcosms differing in matric potential and pore size distribution and, consequently, in connection of micro-habitats via water films. Our sand microcosms were used to examine the individual and competitive responses of a filamentous bacterium (Streptomyces atratus) and a motile rod-shaped bacterium (Bacillus weihenstephanensis) to differences in pore sizes and matric potential. The Bacillus strain had an initial advantage in all sand microcosms, which could be attributed to its faster growth rate. At later stages of the incubation, Streptomyces became dominant in microcosms with low connectivity (coarse pores and dry conditions). These data, combined with information on bacterial motility (expansion potential) across a range of pore-size and moisture conditions, suggest that, like their much larger fungal counterparts, filamentous bacteria also use this growth form to facilitate growth and expansion under conditions of low hydraulic conductivity. The sand microcosm system developed and used in this study allowed for precise manipulation of hydraulic properties and pore size distribution, thereby providing a useful approach for future examinations of how these properties influence the composition, diversity and function of soil-borne microbial communities.
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Vos M, Wolf AB, Jennings SJ, Kowalchuk GA (2013). Micro-scale determinants of bacterial diversity in soil.
FEMS Microbiol Rev,
37(6), 936-954.
Abstract:
Micro-scale determinants of bacterial diversity in soil.
Soil habitats contain vast numbers of microorganisms and harbor a large portion of the planet's biological diversity. Although high-throughput sequencing technologies continue to advance our appreciation of this remarkable phylogenetic and functional diversity, we still have only a rudimentary understanding of the forces that allow diverse microbial populations to coexist in soils. This conspicuous knowledge gap may be partially due the human perspective from which we tend to examine soilborne microorganisms. This review focusses on the highly heterogeneous soil matrix from the vantage point of individual bacteria. Methods describing micro-scale soil habitats and their inhabitants based on sieving, dissecting, and visualizing individual soil aggregates are discussed, as are microcosm-based experiments allowing the manipulation of key soil parameters. We identify how the spatial heterogeneity of soil could influence a number of ecological interactions promoting the evolution and maintenance of bacterial diversity.
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Vos M, te Beek TAH, van Driel MA, Huynen MA, Eyre-Walker A, van Passel MWJ (2013). ODoSE: a webserver for genome-wide calculation of adaptive divergence in prokaryotes.
PLoS One,
8(5).
Abstract:
ODoSE: a webserver for genome-wide calculation of adaptive divergence in prokaryotes.
Quantifying patterns of adaptive divergence between taxa is a major goal in the comparative and evolutionary study of prokaryote genomes. When applied appropriately, the McDonald-Kreitman (MK) test is a powerful test of selection based on the relative frequency of non-synonymous and synonymous substitutions between species compared to non-synonymous and synonymous polymorphisms within species. The webserver ODoSE (Ortholog Direction of Selection Engine) allows the calculation of a novel extension of the MK test, the Direction of Selection (DoS) statistic, as well as the calculation of a weighted-average Neutrality Index (NI) statistic for the entire core genome, allowing for systematic analysis of the evolutionary forces shaping core genome divergence in prokaryotes. ODoSE is hosted in a Galaxy environment, which makes it easy to use and amenable to customization and is freely available at www.odose.nl.
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Vos M, Quince C, Pijl AS, de Hollander M, Kowalchuk GA (2012). A comparison of rpoB and 16S rRNA as markers in pyrosequencing studies of bacterial diversity.
PLoS One,
7(2).
Abstract:
A comparison of rpoB and 16S rRNA as markers in pyrosequencing studies of bacterial diversity.
BACKGROUND: the 16S rRNA gene is the gold standard in molecular surveys of bacterial and archaeal diversity, but it has the disadvantages that it is often multiple-copy, has little resolution below the species level and cannot be readily interpreted in an evolutionary framework. We compared the 16S rRNA marker with the single-copy, protein-coding rpoB marker by amplifying and sequencing both from a single soil sample. Because the higher genetic resolution of the rpoB gene prohibits its use as a universal marker, we employed consensus-degenerate primers targeting the Proteobacteria. METHODOLOGY/PRINCIPAL FINDINGS: Pyrosequencing can be problematic because of the poor resolution of homopolymer runs. As these erroneous runs disrupt the reading frame of protein-coding sequences, removal of sequences containing nonsense mutations was found to be a valuable filter in addition to flowgram-based denoising. Although both markers gave similar estimates of total diversity, the rpoB marker revealed more species, requiring an order of magnitude fewer reads to obtain 90% of the true diversity. The application of population genetic methods was demonstrated on a particularly abundant sequence cluster. CONCLUSIONS/SIGNIFICANCE: the rpoB marker can be a complement to the 16S rRNA marker for high throughput microbial diversity studies focusing on specific taxonomic groups. Additional error filtering is possible and tests for recombination or selection can be employed.
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Vos M (2011). A species concept for bacteria based on adaptive divergence.
Trends Microbiol,
19(1), 1-7.
Abstract:
A species concept for bacteria based on adaptive divergence.
Bacterial strains are currently grouped into species based on overall genomic similarity and sharing of phenotypes deemed ecologically important. Many believe this polyphasic taxonomy is in need of revision because it lacks grounding in evolutionary theory, and boundaries between species are arbitrary. Recent taxonomy efforts using multilocus sequence typing (MLST) data are based on the identification of distinct phylogenetic clusters. However, these approaches face the problem of deciding the phylogenetic level at which clusters are representative of evolutionary or taxonomically distinct units. In this review, I propose classifying two phylogenetic clusters as separate species only when they have statistically significantly diverged as a result of adaptive evolution. More than a method for classification, the concept of adaptive divergence can be used in a 'reverse ecology' approach to identify lineages that are in the process of speciation or genes involved in initial adaptive divergence.
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Garbeva P, Tyc O, Remus-Emsermann MNP, van der Wal A, Vos M, Silby M, de Boer W (2011). No apparent costs for facultative antibiotic production by the soil bacterium Pseudomonas fluorescens Pf0-1.
PLoS One,
6(11).
Abstract:
No apparent costs for facultative antibiotic production by the soil bacterium Pseudomonas fluorescens Pf0-1.
BACKGROUND: Many soil-inhabiting bacteria are known to produce secondary metabolites that can suppress microorganisms competing for the same resources. The production of antimicrobial compounds is expected to incur fitness costs for the producing bacteria. Such costs form the basis for models on the co-existence of antibiotic-producing and non-antibiotic producing strains. However, so far studies quantifying the costs of antibiotic production by bacteria are scarce. The current study reports on possible costs, for antibiotic production by Pseudomonas fluorescens Pf0-1, a soil bacterium that is induced to produce a broad-spectrum antibiotic when it is confronted with non-related bacterial competitors or supernatants of their cultures. METHODOLOGY AND PRINCIPAL FINDINGS: We measured the possible cost of antibiotic production for Pseudomonas fluorescens Pf0-1 by monitoring changes in growth rate with and without induction of antibiotic production by supernatant of a bacterial competitor, namely Pedobacter sp. Experiments were performed in liquid as well as on semi-solid media under nutrient-limited conditions that are expected to most clearly reveal fitness costs. Our results did not reveal any significant costs for production of antibiotics by Pseudomonas fluorescens Pf0-1. Comparison of growth rates of the antibiotic-producing wild-type cells with those of non-antibiotic producing mutants did not reveal costs of antibiotic production either. SIGNIFICANCE: Based on our findings we propose that the facultative production of antibiotics might not be selected to mitigate metabolic costs, but instead might be advantageous because it limits the risk of competitors evolving resistance, or even the risk of competitors feeding on the compounds produced.
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Vos M, Didelot X (2009). A comparison of homologous recombination rates in bacteria and archaea.
ISME J,
3(2), 199-208.
Abstract:
A comparison of homologous recombination rates in bacteria and archaea.
It is a standard practice to test for the signature of homologous recombination in studies examining the genetic diversity of bacterial populations. Although it has emerged that homologous recombination rates can vary widely between species, comparing the results from different studies is made difficult by the diversity of estimation methods used. Here, Multi Locus Sequence Typing (MLST) datasets from a wide variety of bacteria and archaea are analyzed using the ClonalFrame method. This enables a direct comparison between species and allows for a first exploration of the question whether phylogeny or ecology is the primary determinant of homologous recombination rate.
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Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A (2009). Local adaptation of bacteriophages to their bacterial hosts in soil.
Science,
325(5942).
Abstract:
Local adaptation of bacteriophages to their bacterial hosts in soil.
Microbes are incredibly abundant and diverse and are key to ecosystem functioning, yet relatively little is known about the ecological and evolutionary mechanisms that shape their distributions. Bacteriophages, viral parasites that lyse their bacterial hosts, exert intense and spatially varying selection pressures on bacteria and vice versa. We measured local adaptation of bacteria and their associated phages in a centimeter-scale soil population. We first demonstrate that a large proportion of bacteria is sensitive to locally occurring phages. We then show that sympatric phages (isolated from the same 2-gram soil samples as the bacteria) are more infective than are phages from samples some distance away. This study demonstrates the importance of biotic interactions for the small-scale spatial structuring of microbial genetic diversity in soil.
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Vos M, Velicer GJ (2009). Social conflict in centimeter-and global-scale populations of the bacterium Myxococcus xanthus.
Curr Biol,
19(20), 1763-1767.
Abstract:
Social conflict in centimeter-and global-scale populations of the bacterium Myxococcus xanthus.
Social interactions among microbes that engage in cooperative behaviors are well studied in laboratory contexts [1, 2], but little is known about the scales at which initially cooperative microbes diversify into socially conflicting genotypes in nature. The predatory soil bacterium Myxococcus xanthus responds to starvation by cooperatively forming multicellular fruiting bodies in which a portion of the population differentiates into stress-resistant spores [3, 4]. Natural M. xanthus populations are spatially structured [5], and genetically divergent isolates from distant origins exhibit striking developmental antagonisms that decrease spore production in chimeric fruiting bodies [6]. Here we show that genetically similar isolates of M. xanthus from a centimeter-scale population [7] also exhibit strong and pervasive antagonisms when mixed in development. Negative responses to chimerism were less intense on average among local strains than among global isolates, although no significant correlation was found between genetic distance at multilocus sequence typing (MLST) loci and the degree of social asymmetry between competitors. A test for self/nonself discrimination during vegetative swarming revealed a great diversity of distinct self-recognition types even among identical MLST genotypes. Such nonself exclusion may serve to direct the benefits of cooperation to close kin within diverse populations in which the probability of social conflict among neighbors is high.
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Velicer GJ, Vos M (2009). Sociobiology of the Myxobacteria.
ANNUAL REVIEW OF MICROBIOLOGY,
63, 599-623.
Author URL.
Vos M (2009). Why do bacteria engage in homologous recombination?.
Trends Microbiol,
17(6), 226-232.
Abstract:
Why do bacteria engage in homologous recombination?
Microbiologists have long recognized that the uptake and incorporation of homologous DNA from outside the cell is a common feature of bacteria, with important implications for their evolution. However, the exact reasons why bacteria engage in homologous recombination remain elusive. This Opinion article aims to reinvigorate the debate by examining the costs and benefits that homologous recombination could engender in natural populations of bacteria. It specifically focuses on the hypothesis that homologous recombination is selectively maintained because the genetic variation it generates improves the response of bacterial populations to natural selection, analogous to sex in eukaryotes.
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Krug D, Zurek G, Revermann O, Vos M, Velicer GJ, Müller R (2008). Discovering the hidden secondary metabolome of Myxococcus xanthus: a study of intraspecific diversity.
Applied and Environmental Microbiology,
74(10), 3058-3068.
Abstract:
Discovering the hidden secondary metabolome of Myxococcus xanthus: a study of intraspecific diversity
As a monophyletic group, the myxobacteria are known to produce a broad spectrum of secondary metabolites. However, the degree of metabolic diversity that can be found within a single species remains unexplored. The model species Myxococcus xanthus produces several metabolites also present in other myxobacterial species, but only one compound unique to M. xanthus has been found to date. Here, we compare the metabolite profiles of 98 M. xanthus strains that originate from 78 locations worldwide and include 20 centimeter-scale isolates from one location. This screen reveals a strikingly high level of intraspecific diversity in the M. xanthus secondary metabolome. The identification of 37 nonubiquitous candidate compounds greatly exceeds the small number of secondary metabolites previously known to derive from this species. These results suggest that M. xanthus may be a promising source of future natural products and that thorough intraspecific screens of other species could reveal many new compounds of interest. Copyright © 2008, American Society for Microbiology. All Rights Reserved.
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Vos M, Velicer GJ (2008). Isolation by Distance in the Spore-Forming Soil Bacterium Myxococcus xanthus. Current Biology, 18(10).
Vos M, Velicer GJ (2008). Isolation by distance in the spore-forming soil bacterium <i>Myxococcus xanthus</i>.
CURRENT BIOLOGY,
18(5), 386-391.
Author URL.
Vos M, Velicer GJ (2008). Natural variation of gliding motility in a centimetre-scale population of Myxococcus xanthus.
FEMS Microbiology Ecology,
64(3), 343-350.
Abstract:
Natural variation of gliding motility in a centimetre-scale population of Myxococcus xanthus
A major challenge in microbial evolutionary ecology is to understand how fitness-related traits vary in natural populations of microorganisms at defined spatial scales and subsequently to identify the forces that maintain such variation. The Gram-negative soil bacterium Myxococcus xanthus is a model system for the study of gliding motility, which is driven by two complementary motility systems in this species and is central to its social lifestyle. We tested whether the ecological context of a centimetre-scale M. xanthus population allows the coexistence of diverse motility-related phenotypes. Swarming rates among 26 clones isolated at the centimetre scale were found to vary greatly in multiple laboratory environments. This variation appears to be motility-specific, as it is not explained by a correlated variation in intrinsic growth rate. In contrast to the common reference strain DK1622, most isolates swarmed faster on hard agar than on soft agar, highlighting the difficulty of inferring species characteristics from laboratory reference strains. These isolates also varied greatly in swarm morphology and in the effect of nutrient limitation on swarming rate. Our results show that diverse swarming phenotypes can coexist in a small-scale bacterial population. © 2008 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.
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Buckling A, Harrison F, Vos M, Brockhurst MA, Gardner A, West SA, Griffin A (2007). Siderophore‐mediated cooperation and virulence in Pseudomonas aeruginosa. FEMS Microbiol Ecol, 62, 135-141.
Harrison F, Browning LE, Vos M, Buckling A (2006). Cooperation and virulence in acute Pseudomonas aeruginosa infections.
BMC Biol,
4Abstract:
Cooperation and virulence in acute Pseudomonas aeruginosa infections.
BACKGROUND: Efficient host exploitation by parasites is frequently likely to depend on cooperative behaviour. Under these conditions, mixed-strain infections are predicted to show lower virulence (host mortality) than are single-clone infections, due to competition favouring non-contributing social 'cheats' whose presence will reduce within-host growth. We tested this hypothesis using the cooperative production of iron-scavenging siderophores by the pathogenic bacterium Pseudomonas aeruginosa in an insect host. RESULTS: We found that infection by siderophore-producing bacteria (cooperators) results in more rapid host death than does infection by non-producers (cheats), and that mixtures of both result in intermediate levels of virulence. Within-host bacterial growth rates exhibited the same pattern. Crucially, cheats were more successful in mixed infections compared with single-clone infections, while the opposite was true of cooperators. CONCLUSION: These data demonstrate that mixed clone infections can favour the evolution of social cheats, and thus decrease virulence when parasite growth is dependent on cooperative behaviours.
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Vos M, Velicer GJ (2006). Genetic Population Structure of the Soil Bacterium Myxococcus xanthus at the Centimeter Scale.
Appl Environ Microbiol,
72, 3615-3625.
Abstract:
Genetic Population Structure of the Soil Bacterium Myxococcus xanthus at the Centimeter Scale
Myxococcus xanthus is a gram-negative soil bacterium best known for its remarkable life history of social swarming, social predation, and multicellular fruiting body formation. Very little is known about genetic diversity within this species or how social strategies might vary among neighboring strains at small spatial scales. To investigate the small-scale population structure of M. xanthus, 78 clones were isolated from a patch of soil (16 by 16 cm) in Tubingen, Germany. Among these isolates, 21 genotypes could be distinguished from a concatemer of three gene fragments: csgA (developmental C signal), fibA (extracellular matrix-associated zinc metalloprotease), and pilA (the pilin subunit of type IV pili). Accumulation curves showed that most of the diversity present at this scale was sampled. The pilA gene contains both conserved and highly variable regions, and two frequency-distribution tests provide evidence for balancing selection on this gene. The functional domains in the csgA gene were found to be conserved. Three instances of lateral gene transfer could be inferred from a comparison of individual gene phylogenies, but no evidence was found for linkage equilibrium, supporting the view that M. xanthus evolution is largely clonal. This study shows that M. xanthus is surrounded by a variety of distinct conspecifics in its natural soil habitat at a spatial scale at which encounters among genotypes are likely.
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