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Hesse, E.

Publications and source records attributed to Hesse, E..

18 recordsLinked to original sources

Sign and strength of pairwise interactions in natural isolates depend on environment type.

Bacterial interactions-whether positive or negative - are crucial for the functioning of microbial communities. Though bacterial interactions are mainly expected to be negative, the sign and strength of interactions are predicted to be context dependent, with interactions typically being more positive in more stressful and nutrient-poor conditions. However, systematic studies investigating how the environment affects interactions between multiple taxa are lacking. Here, we determine if interactions between a panel of natural soil isolates change in response to the environment in which they are grown, with two different artificial media used (one simple and one complex) and a more ecologically relevant soil wash. To maximise natural variation in interactions, we collected multiple isolates from multiple sites: co-occurring (sympatric) isolates were predicted to show more negative interactions than allopatric isolates because of greater overlap in resource use. Pairwise interactions were in general negative, but more negative when grown in a complex lab-derived medium (Tryptic Soy Broth). Mutually beneficial interactions were most common in a simple resource medium (M9 minimal media) and exploitative interactions were most frequent in a soil broth. These patterns were independent of whether species originated from the same or a different site. The study supports the prediction that nutrient rich environments promote more negative interactions, and that measuring interactions of soil isolates in standard lab media is likely to misrepresent interactions occurring in natural environments.

microbiology↗

Community complexity does not weaken pairwise coevolution in a soil bacterial community

Exploitative interactions, such as predator-prey and host-parasite interactions, are ubiquitous in microbial communities. These interactions shape community density and composition, imposing strong selection on members to evolve countermeasures reducing the negative impacts of exploitation. Exploitative coevolution is often studied between species pairs in isolation, which may over-estimate the strength and relevance of pairwise coevolution. Here we studied how community context influences coevolution between Pseudomonas fluorescens (exploited) and Variovorax sp. (exploiter). We evolved these species in pairwise coculture and embedded within a five-species community to investigate evolved changes in pairwise interactions. We found evidence for asymmetrical coevolution: Variovorax evolved more rapidly than Pseudomonas, leading to increased exploitation through time, while Pseudomonas evolved increased tolerance to Variovorax with time lag. The pairwise coevolutionary dynamics were not affected by the presence of other community members. Understanding how coevolutionary patterns change with increasing community complexity can have important implications for community persistence and function.

evolutionary biology↗

Competition between plasmids conferring the same antimicrobial resistance leads to plasmid-host network specialisation

Plasmids have a key role in disseminating antimicrobial resistance (AMR). Previous work has shown that in the presence of antibiotics, plasmids conferring AMR will spread to a larger number and a more phylogenetically diverse group of host organisms. However, this pattern may be complicated when multiple plasmids confer the same resistance. Here, we analyse host-plasmid networks in experimental communities of three bacterial species cultured for six weeks with three incompatible plasmids (plasmids that cannot stably coexist within a single cell) conferring tetracycline resistance. The communities are cultured either without tetracycline, or with a low or high dose of the antibiotic. We find that while antibiotic selection leads to higher plasmid prevalence, it does not change the structure of host-plasmid networks. Under all conditions, the networks become highly specialised, as specific host-plasmid pairings emerge. This result is supported by a previously published mathematical model parameterised to match our experimental set-up. Our study reiterates the importance of fitness effects of plasmids in determining the structure of bacteria-plasmid networks. The spread of a given AMR plasmid is reduced when fitness differences are reduced due to other plasmids carrying AMR genes, leading to more specialised bacteria-plasmid networks.

microbiology↗

Cheats can boost the success of a cooperative invader

Successful biological invasions are dependent on the invader being able to grow and reproduce in the new environment. One way that microbial invaders may facilitate this is to use cooperative public goods, such as metal-binding siderophores. However, siderophore production can be exploited by non-producing cheats who benefit from production without paying any associated costs. Here, we test the importance of cooperation for the success of Pseudomonas aeruginosa invading a 5-species microbial community. We do this by comparing the success of a siderophore-producing strain, a siderophore-deficient mutant strain and a 50:50 mixed population, both in environments with weak (copper absent) and strong (copper present) siderophore requirement. We found no effect of invader type on success when siderophores were less essential for growth, but large differences when they were selectively favoured. Here the producer-cheat mix had the greatest success, with both strains having near equal fitness and reaching high densities, whilst in isolation producers had intermediate success and cheats the lowest. Similarly, resident diversity only differed across invader treatments when copper was present. In conclusion, we show that the presence of cheats can provide a larger benefit for invasion success than pure cooperator populations, but only when public goods are particularly beneficial.

ecology↗

TAM receptors control actomyosin dynamics in osteoclasts via RHOA-COFILIN-MYOSIN II signaling

The TAM family of receptor tyrosine kinases were recently identified to regulate bone homeostasis by controlling osteoblasts and bone formation. Despite extensive knowledge of TAM receptor function in the mononuclear phagocyte system, the role of TAM receptors in osteoclasts remains largely unknown. Here, we identify a physiological regulatory system including MERTK and TYRO3 in osteoclasts controlling RHOA-ROCK-COFILIN/Myosin II signaling, thereby antagonistically regulating osteoclast-mediated bone remodeling to maintain bone homeostasis. Myeloid-specific lysozyme M-mediated deletion of Mertk led to increased bone mass in mice. In early stages of RANKL-induced osteoclast differentiation MERTK promotes amoeboid migration mode in osteoclast precursor cells by inducing RHOA-COFILIN-MLC2 pathway leading to increased osteoclast formation. In contrast, TYRO3 inhibits RHOA-ROCK signaling in osteoclast precursor cells thereby inhibiting these processes. Furthermore, we unraveled an inhibitory role of MERTK as well as TYRO3 in osteoclast differentiation and function. In line with this, mice with cathepsin K-mediated deletion of Mertk and Tyro3 exhibited an osteoporotic bone phenotype. We found that osteoclast precursor cell morphology dictates its fusion capacity and identified MERTK as a negative regulator of osteoclast fusion. In multinucleated cells, deletion of Mertk inhibits actin ring formation by mediating central actomyosin contraction and inactivation of COFILIN. In contrast, spatially well-ordered RHOA activation at adhesion structures, induced by loss of Tyro3, improves osteoclast biomechanotransduction to ameliorate podosome belt formation and enhance osteoclast function. By using a syngeneic breast cancer bone metastasis osteolysis models we identified TYRO3 as a bone protective receptor for osteolytic bone diseases, whereas MERTK represents a pharmacologic accessible target to inhibit osteoclast formation because its stimulatory effects of osteoclast precursors prevail the inhibitory effects on mature osteoclasts. Next to the recently uncovered role of MERTK as a target for osteoanabolic therapy MERTK may represent a one-drug two-target treatment strategy to increase osteoblast function and reduce osteoclast formation for treatments of bone diseases.

cell biology↗

Disturbances can facilitate prior invasions more than subsequent invasions in microbial communities

Invasions by microorganisms are commonly found to benefit from disturbance events. However, the importance of the relative timing and order of the invasion and disturbance for invader success remains uncertain. Here, by invading a stably coexisting community of five bacterial species at four different propagule pressures on eight separate occasions - four pre-disturbance and four post-disturbance - we experimentally tested the importance of timing and order for the invaders success. Furthermore, we quantified the impact of the invader on the composition of the resident community. Across a range of invader densities, both pre- and post-disturbance invader success was greatest the closer in time to the disturbance. While the greatest invasion success occurred when the invasion immediately followed the disturbance, invasion resistance rapidly recovered, such that the three subsequent invasions had negligible success. As a consequence, overall invader success was greatest pre-than post-disturbance. We found that invasion day as well as success significantly affected resident diversity, such that it was lowest in communities invaded immediately after the disturbance, but was overall lower in communities invaded pre-disturbance. Overall, these results demonstrate that invading immediately after a disturbance is highly beneficial for invader success and results in the biggest change to community composition. Importantly however, they also show that this window of opportunity is very brief, and that, on average, an invader will have a greater success and effect on community composition if it invades before a disturbance.

ecology↗

Tgif1-deficiency impairs cytoskeletal architecture in osteoblasts by suppressing PAK3 signaling

Osteoblast adherence to bone surfaces is important for remodeling of the bone tissue. This study demonstrates that deficiency of TG-interacting factor 1 (Tgif1) in osteoblasts results in altered cell morphology, reduced adherence to collagen type I-coated surfaces, and impaired migration capacity. Tgif1 is essential for osteoblasts to adapt a regular cell morphology and to efficiently adhere and migrate on collagen type I-rich matrices in vitro. Furthermore, Tgif1 acts as transcriptional repressor of p21-activated kinase 3 (PAK3), an important regulator of focal adhesion formation and osteoblast spreading. Absence of Tgif1 leads to increased PAK3 expression, which impairs osteoblast spreading. Additionally, Tgif1 is implicated in osteoblast recruitment and activation of bone surfaces in the context of bone regeneration and in response to parathyroid hormone 1-34 (PTH 1-34) treatment in vivo. These findings provide important novel insights in the regulation of the cytoskeletal architecture of osteoblasts.

cell biology↗

Copper reduces the virulence of bacterial communities at environmentally relevant concentrations

Increasing environmental concentrations of metals as a result of anthropogenic pollution are significantly changing many microbial communities. While there is evidence metal pollution can result in increased antibiotic resistance, the effects of metal pollution on virulence remains largely undetermined. Here, we experimentally test whether metal stress alters the virulence of bacterial communities. We do this by incubating three wastewater influent communities under different environmentally relevant copper concentrations for three days. We then quantify the virulence of the community using the Galleria mellonella infection model, and test if differences are due to changes in the rate of biomass accumulation (productivity), copper resistance, or community composition (quantified using 16S amplicon sequencing). The virulence of the communities was found to be reduced by the highest copper concentration, but not to be affected by the lower concentration. As well as reduced virulence, communities exposed to the highest copper concentration were less diverse and had lower productivity. This work highlights that metal pollution may decrease virulence in bacterial communities, but at a cost to diversity and productivity.

microbiology↗

The effect of metal remediation on the virulence and antimicrobial resistance of the opportunistic pathogen Pseudomonas aeruginosa

Metal contamination poses both a direct threat to human health as well as an indirect threat through its potential to affect bacterial pathogens. Metals can not only co-select for antibiotic resistance, but also might affect pathogen virulence via increased siderophore production. Siderophores are extracellular compounds released to increase ferric iron uptake -- a common limiting factor for pathogen growth within hosts - making them an important virulence factor. However, siderophores can also be positively selected for to detoxify non-ferrous metals, and consequently metal stress can potentially increase bacterial virulence. Anthropogenic methods to remediate environmental metal contamination commonly involve amendment with lime-containing materials, but whether this reduces in situ co-selection for antibiotic resistance and virulence remains unknown. Here, using microcosms containing metal-contaminated river water and sediment, we experimentally test whether metal remediation by liming reduces co-selection for these traits in the opportunistic pathogen Pseudomonas aeruginosa embedded within a natural microbial community. To test for the effects of environmental structure, which can 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, but this effect was reduced in the limed treatments. Evolved P. aeruginosa populations 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. We therefore demonstrate that although remediation via liming reduced the strength of selection for metal resistance mechanisms, it 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. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=77 SRC="FIGDIR/small/508257v2_ufig1.gif" ALT="Figure 1"> View larger version (23K): org.highwire.dtl.DTLVardef@2f396corg.highwire.dtl.DTLVardef@62e7b3org.highwire.dtl.DTLVardef@159d269org.highwire.dtl.DTLVardef@52395_HPS_FORMAT_FIGEXP M_FIG C_FIG

ecology↗

Copper selects for siderophore-mediated virulence in Pseudomonas aeruginosa

Iron 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.

ecology↗

Short-term relative invader growth rate predicts long-term equilibrium proportion in a stable, coexisting microbial community

Model microbial communities are regularly used to test ecological and evolutionary theory as they are easy to manipulate and have fast generation times, allowing for large-scale, high throughput experiments. A key assumption for most model microbial communities is that they stably coexist, but this is rarely tested experimentally. Here we report the (dis)assembly of a five-species microbial community from a metacommunity of soil microbes that can be used for future experiments. Using reciprocal invasion from rare experiments we show that all species can coexist and we demonstrate that the community is stable for a long time ([~]600 generations). Crucially for future work, we show that each species can be identified by their plate morphologies, even after >1 year in co-culture. We characterise pairwise species interactions and produce high-quality reference genomes for each species. This stable five-species community can be used to test key questions in microbial ecology and evolution.

ecology↗

Zinc can counteract selection for ciprofloxacin resistance

Antimicrobial 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-resistant Escherichia coli MG1655 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.\n\nGraphical abstract\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=150 SRC=\"FIGDIR/small/780981v1_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (23K):\norg.highwire.dtl.DTLVardef@9abc9eorg.highwire.dtl.DTLVardef@d54d48org.highwire.dtl.DTLVardef@1c4df88org.highwire.dtl.DTLVardef@2f67f6_HPS_FORMAT_FIGEXP M_FIG C_FIG One sentence summaryThe minimal selective concentration for a ciprofloxacin resistant E. coli strain increases up to 5-fold in the presence of Zinc cations.

microbiology↗

Interspecific social interactions shape public goods production in natural microbial communities

Evolution can occur over ecological timescales, suggesting a potentially important role for rapid evolution in shaping community trait distributions. However, evidence of concordant eco-evolutionary dynamics often comes from in vitro studies of highly simplified communities, and measures of ecological and evolutionary dynamics are rarely directly comparable. Here, we quantified how ecological species sorting and rapid evolution simultaneously shape community trait distributions by tracking within and between-species changes in a key trait in a complex bacterial community. We focused on the production of siderophores; bacteria use these costly secreted metabolites to scavenge poorly soluble iron and to detoxify environments polluted with toxic non-ferrous metals. We found that responses to copper-imposed selection within and between species were ultimately the same - intermediate siderophore levels were favored - and occurred over similar timescales. Despite being a social trait, this level of siderophore production was selected regardless of whether species evolved in isolation or in a community context. Our study suggests that evolutionary selection can play a pivotal role in shaping community trait distributions within natural, highly complex, bacterial communities. Furthermore, trait evolution may not always be qualitatively affected by interactions with other community members. SignificanceBacterial communities possess remarkable taxonomic and metabolic diversity and play a key role in nearly every biogeochemical process on Earth. Rapid evolution (occurring over ecological time scales) can in principle shape these processes, yet we have little understanding of its importance in natural communities. Here, we quantified how the production of metal-detoxifying siderophores is driven by species compositional changes and evolution in a compost community in response to copper stress. We found that siderophore production converged at intermediate levels, with evolutionary and ecological changes occurring at similar rates. Understanding how ecological and evolutionary processes contribute to shaping trait distributions will improve our ability to predict ecosystem responses to global change, and aid in the engineering of microbial consortia.

evolutionary biology↗

Short-term evolution under copper stress increases probability of plasmid uptake

Understanding plasmid transfer dynamics remains a key knowledge gap in the mitigation of antibiotic resistance gene spread. Direct effects of exposure to stressors on plasmid uptake are well monitored. However, it remains untested whether evolution of strains under stress conditions modulates subsequent plasmid uptake. Here, we evolved a compost derived microbial community for six weeks under copper stress and non-exposed control conditions. We then tested the ability of isolated clones from both treatments to take up the broad host range plasmid pKJK5 from an E.coli donor strain. Clones pre-adapted to copper displayed a significantly increased probability to be permissive towards the plasmid compared to those isolated from the control treatment. Further, increased phylogenetic distance to the donor strain was significantly and negatively correlated with plasmid uptake probabilities across both treatments.

microbiology↗

Anthropogenic remediation of heavy metals selects against natural microbial remediation

In an era of unprecedented environmental change, there have been increasing ecological and global public health concerns associated with exposure to anthropogenic pollutants. While there is a pressing need to remediate polluted ecosystems, human intervention strategies might unwittingly oppose selection for natural detoxification, which is primarily carried out by microbes. We test this possibility in the context of a ubiquitous chemical remediation strategy aimed at targeting toxic metal pollution: the addition of lime-containing materials. Here we show that raising pH by liming decreased the availability of toxic metals in acidic mine-degraded soils, but as a consequence selected against microbial taxa that naturally remediate soil through the production of metal-scavenging siderophores. Understanding the ecological and evolutionary consequences of human intervention on key traits is crucial for the engineering of evolutionary resilient microbial communities, having important implications for human health and biotechnology.

ecology↗

Glucosinolates promote initial population establishment of feral oilseed rape

BackgroundCrops are often selected for traits that confer a selective disadvantage in the wild. A key trait that has been greatly altered by domestication is investment in herbivore defence. It remains unclear, however, whether variation in chemical defence affects a crops ability to colonize semi-natural habitats where it typically has to compete with a resident community. Here, we investigate how breeding efforts aimed at reducing glucosinolate levels in seeds - canonical herbivore deterrents - influence initial establishment of Brassica populations spanning a wild-feral-domesticated gradient.\n\nMethodsWe followed the dynamics of twenty-nine Brassica accessions in two experimental fields by recording life table parameters and vegetation cover biannually over a two-year period. Accessions were selected to vary in their glucosinolate content, and included lines of wild turnip (B. rapa), feral B. napus as well as modern canola and historical oilseed rape cultivars. Populations were established by sowing seeds on bare soil after which the natural vegetation was allowed to regenerate, providing a temporal gradient in the degree of interspecific competition.\n\nResultsPopulations flourished in the first year, but many perished during a second year of growth, in particular those of oilseed rape. Declines coincided with an increase in vegetation cover, but were slower in populations harbouring more glucosinolates. These compounds had opposing effects on different life cycle stages: seedling establishment was greater in high-glucosinolate lines, which traded off with reduced post-recruitment survival. Crucially, the effect of glucosinolates on persistence was lost when focussing on oilseed rape only, but the underlying demographic trade-off remained.\n\nDiscussionOur study illustrates that initial establishment of feral oilseed rape is governed by glucosinolate-mediated trade-offs between seedling recruitment and subsequent survival, with low-glucosinolate lines (modern canola) being most successful when post-recruitment conditions are relatively benign. Such demographic trade-offs likely extend to other species, and must be considered when managing escaped crops and invasive plants.

ecology↗

Using the Wax moth larva Galleria mellonella infection model to detect emerging bacterial pathogens

Climate change, changing farming practices, social and demographic changes and rising levels of antibiotic resistance are likely to lead to future increases in opportunistic bacterial infections that are more difficult to treat. Uncovering the prevalence and identity of pathogenic bacteria in the environment is key to assessing transmission risks. We describe the first use of the Wax moth larva Galleria mellonella, a well-established model for the mammalian innate immune system, to selectively enrich and characterize pathogens from coastal environments in the South West of the U.K. Whole-genome sequencing of highly virulent isolates revealed amongst others a Proteus mirabilis strain carrying the Salmonella SGI1 genomic island not reported from the U.K. before and the recently described species Vibrio injenensis hitherto only reported from human patients in Korea. Our novel method has the power to detect novel bacterial pathogens in the environment that potentially pose a serious risk to public health.

microbiology↗

Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination

Some microbial public goods can provide both individual and community-wide benefits, and are open to exploitation by non-producing species. One such example is the production of metal-detoxifying siderophores. Here, we investigate whether heavy metals select for increased siderophore production in natural microbial communities, or whether exploitation of this detoxifying effect reduces siderophore production. We show that the proportion of siderophore-producing taxa increases along a natural heavy metal gradient. A causal link between metal contamination and siderophore production was subsequently demonstrated in a microcosm experiment in compost, in which we observed changes in community composition towards taxa that produce relatively more siderophores following copper contamination. We confirmed the selective benefit of siderophores by showing that taxa producing large amount of siderophores suffered less growth inhibition in toxic copper. Our results suggest that ecological selection will favour siderophore-mediated decontamination, with important consequences for potential remediation strategies.\n\nAuthorshipEH, SOB, AL, DJH, EvV, AB conceived and designed the experiment. DJH provided new perspectives. EH, SOB, FB, AL collected the data. EH, FB, NT, DJH carried out the data analyses. EH & AB wrote the first draft of the manuscript, and all authors contributed substantially to revisions.\n\nData accessibilityUpon acceptance, data presented in the manuscript will be made available on Dryad.

ecology↗