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Ramoneda, J.

Publications and source records attributed to Ramoneda, J..

11 recordsLinked to original sources

A life-history axis of resource acquisition in bacteria: depolymerisation versus uptake

Microbial decomposition of complex organic matter is a major control on the global carbon cycle, and its efficiency hinges on how microbes acquire resources. Decomposition requires costly extracellular enzymes to break down complex polymers, whereas the resulting soluble products are captured far more cheaply through membrane transporters. How microbes balance investment between these two processes is a fundamental axis of microbial life history, yet it has remained difficult to quantify across their vast diversity. Using genomic repertoires for carbohydrate depolymerisation and uptake, we developed a simple ratio distinguishing depolymerisation-optimised from uptake-optimised strategies, and applied it to more than 249,000 environmental and host-associated bacterial genomes. These strategies were strongly phylogenetically structured and differed by habitat, with uptake-optimised bacteria unexpectedly more prevalent in diffusion-limited soils than in aquatic environments. In an 18-month field-scale plant litter decomposition experiment, uptake-optimised bacteria dominated during early decomposition, when fungi were more abundant and strongly expressed hydrolytic enzymes, shifting towards depolymerisation-optimised bacteria at later stages. A simple genomic ratio therefore captures ecologically meaningful resource-acquisition strategies that vary with phylogeny, habitat and successional stage. The balance of these strategies could shape community-level extracellular enzyme investment, with consequences for decomposition and carbon cycling.

microbiology↗

Environmental sensing capacity predicts bacterial ecological strategies and environmental preferences

The ability to sense environmental variation is a prerequisite for ecological success. Sensor domains enable bacteria to detect nutrients, neighboring organisms, and physicochemical conditions, but whether variation in these sensing systems reflects ecological specialization remains unresolved. Here, we analyzed sensor domains across 51,343 bacterial genomes and 255 soil metagenomes spanning a climatic gradient to determine whether sensory repertoires encode bacterial ecological strategies and environmental preferences. Sensory repertoires exhibited strong phylogenetic conservatism and revealed signatures of genome streamlining, indicating that environmental sensing reflects trade-offs associated with maintaining sensory complexity. Taxa occupying environmentally heterogeneous habitats, particularly free-living aerobic generalists, encoded the largest sensory repertoires, consistent with selection for expanded environmental information processing. To link sensory function with ecological adaptation, we mapped experimentally-characterized ligand-binding motifs (LBMs) across genomes and metagenomes. Distinct LBM profiles discriminated host-associated and free-living taxa, aerobic and anaerobic lineages, and generalists and non-generalists, revealing a tight coupling between sensory capacity and ecological strategy. Across soil communities, motifs associated with osmoprotection and oxygen sensing were consistently enriched under increasing aridity, linking sensory function to environmental filtering in natural ecosystems. These findings identify environmental sensing as an important organizational axis of bacterial trait-based ecology that integrates evolutionary history, ecological lifestyle, and adaptation to local conditions. Environmental sensing should be considered for predicting microbial niches and responses to environmental change.

ecology↗

Plasmid transfer and loss probabilities interactively determine antibiotic resistance spread in surface-associated bacterial biomass

Plasmid transfer among bacteria is an evolutionary driver of the spread of antibiotic resistance. Surface-associated bacterial biomass is a hotspot for plasmid transfer due to the dense spatial packing of cells. Compared to plasmid dynamics within a single biomass unit, the determinants of plasmid transfer between discrete units are less understood. Yet, discrete units routinely physically collide with each other as they grow, such as in sparse biofilms. Here, we used individual-based modelling to quantitatively predict how the probabilities of plasmid transfer and loss affect plasmid spread between discrete bacterial colonies as they grow and physically collide into each other. We found that these factors have interactive effects on the extent of plasmid transfer and the subsequent proliferation of transconjugants. We further found that these effects are controlled by the spatial distance between the colliding colonies and the spatial positioning of plasmid-carrying cells along the collision boundary. We then experimentally tested our modelling predictions using strains of Pseudomonas stutzeri and Escherichia coli that can exchange an antibiotic resistance-encoding plasmid. Our study reveals that plasmid transfer between colliding biomass units is determined by the complex interplay between plasmid transfer, plasmid loss, and spatial constraints, expanding our understanding of plasmid dynamics.

microbiology↗

The ecological relevance of flagellar motility in soil bacterial communities

Flagellar motility is a key bacterial trait as it allows bacteria to navigate their immediate surroundings. Not all bacteria are capable of flagellar motility, and the distribution of this trait, its ecological associations, and the life history strategies of flagellated taxa remain poorly characterized. We developed and validated a genome-based approach to infer the potential for flagellar motility across 12 bacterial phyla (26,192 genomes in total). The capacity for flagellar motility was associated with a higher prevalence of genes for carbohydrate metabolism and higher maximum potential growth rates, suggesting that flagellar motility is more prevalent in resource-rich environments due to the energetic costs associated with this trait. To test this hypothesis, we focused on soil bacterial communities, where flagellar motility is expected to be particularly important given the heterogeneous nature of the soil environment. We applied a method to infer the prevalence of flagellar motility in whole bacterial communities from metagenomic data, and quantified the prevalence of flagellar motility across 4 independent field studies that each captured putative gradients in soil carbon availability (148 metagenomes). As expected, we observed a positive relationship between the prevalence of bacterial flagellar motility and soil carbon availability in each of these datasets. Given that soil carbon availability is often correlated with other factors that could influence the prevalence of flagellar motility, we validated these observations using metagenomic data acquired from a soil incubation experiment where carbon availability was directly manipulated with glucose amendments, confirming that the prevalence of bacterial flagellar motility is consistently associated with soil carbon availability over other potential confounding factors. Flagellar motility is a fundamental phenotypic trait for bacterial adaptation to soil, defining life history strategies primarily associated with resource availability. More generally, this work highlights the value of combining genomic and metagenomic approaches to expand our understanding of microbial phenotypic traits and reveal their general environmental associations.

ecology↗

Timing of antibiotic administration determines the spread of plasmid-encoded antibiotic resistance during microbial range expansion

The spread of antibiotic resistance (AR) is a major threat to global health. Plasmid-mediated horizontal gene transfer is the main mechanism by which AR is transferred between cells lying within close spatial proximity to each other. In this study, we address a fundamental question regarding the spread of AR-encoding plasmids: Is there an optimal time to administer antibiotics to minimize plasmid spread within microbial communities? We addressed this question using microbial consortia consisting of two Pseudomonas stutzeri strains, where one is an AR-encoding plasmid donor and the other a potential recipient. We allowed the strains to co-expand across a nutrient-amended surface and administered antibiotics at different points in time. We found that the extents of plasmid transfer and transconjugant proliferation have unimodal relationships with the timing of antibiotic administration, where they reach maxima at intermediate administration times. Using an individual-based model, we found that these unimodal relationships result from an interplay between the probability to acquire plasmids from neighboring cells and the probability of plasmid loss upon cell division. Our study provides novel mechanistic insights into the transfer and proliferation of AR-encoding plasmids within microbial communities and identifies the timing of antibiotic administration as an important determinant of AR spread.

microbiology↗

Physical contacts between sparse biofilms promote plasmid transfer and generate functional novelty

The horizontal transfer of plasmids is an important driver of microbial evolution, such as conferring antibiotic resistance (AR) to new genotypes. In biofilms, the abundance of cell-cell contacts promotes the frequent transfer of plasmids and their associated genes. In this study, we expand our knowledge about AR-encoding plasmids by investigating their transfer between discrete biofilms as the biofilms grow and physically collide with each other. Using an experimental system consisting of two fluorescently labelled Pseudomonas stutzeri strains and an Escherichia coli strain, we show that biofilm collisions promote plasmid transfer along the collision boundaries. The extent of plasmid transfer depends on the plasmid loss probability, the plasmid transfer probability, and the relative growth rates of plasmid-free and plasmid-carrying cells. We further show that the proliferation of plasmids after biofilm collision depends on the spatial positionings of plasmid-carrying cells along the collision boundary, thus establishing a link between the large-scale spatial distribution of discrete biofilms and the small-scale spatial arrangement of cells within individual biofilms. Our study reveals that plasmid transfer during biofilm collisions is determined by spatial factors operating at different organizational levels and length scales, expanding our understanding of the fate of plasmid-encoded traits in microbial communities.

microbiology↗

Building a genome-based understanding of bacterial pH preferences

The environmental preferences of many microbes remain undetermined. This is the case for bacterial pH preferences, which can be difficult to predict a priori despite the importance of pH as a factor structuring bacterial communities in many systems. We compiled data on bacterial distributions from five datasets spanning pH gradients in soil and freshwater systems (1470 samples in total), quantified the pH preferences of bacterial taxa across these datasets, and compiled genomic data from representative bacterial taxa. While taxonomic and phylogenetic information were generally poor predictors of bacterial pH preferences, we identified genes consistently associated with pH preference across environments. We then developed and validated a machine learning model to estimate bacterial pH preferences from genomic information alone, a model which could aid in the selection of microbial inoculants, improve species distribution models, or help design effective cultivation strategies. More generally, we demonstrate the value of combining biogeographic and genomic data to infer and predict the environmental preferences of diverse bacterial taxa.

ecology↗

Environmental controls and habitat connectivity of phototrophic microbial mats and bacterioplankton communities in an Antarctic freshwater system

Freshwater ecosystems are considered hotspots of biodiversity in Antarctic polar deserts. Anticipated warming is expected to change the hydrology of these systems due to increased meltwater and reduction of ice cover, with implications for environmental conditions and physical connectivity between habitats. Using 16S rRNA sequencing, we evaluated the structure of microbial mat and planktonic communities within a connected watershed in the McMurdo Wright Valley, Antarctica to determine the roles of connectivity and habitat conditions in controlling microbial assemblage composition. We examined benthic and planktonic samples from glacial Lake Brownworth, the perennially ice-covered Lake Vanda, and the Onyx River, which connects the two. In Lake Vanda, we found distinct microbial assemblages occupying sub-habitats at different lake depths, while the communities from Lake Brownworth and Onyx River were structurally similar between them. Despite the higher connectivity between bacterial communities in the shallow parts of the system, environmental filtering dominated over dispersal in driving bacterial community structure. Functional metagenomics predictions identified genes related to degradation of halogenated aromatic compounds in surface microbial mats exposed to changes in water regimes, which progressively disappeared with increasing depth. Shifting environmental conditions due to increasing connectivity, rather than dispersal, may become the dominant drivers of bacterial diversity and functioning in Antarctic freshwater ecosystems.

ecology↗

Ecological patterns of root nodule diversity in cultivated and wild rooibos populations: a community prediction approach

There is interest in understanding the factors behind the biogeography of root-associated bacteria due to the joint effects that plant host, climate, and soil conditions can have on bacterial diversity. For legume crops with remaining wild populations, this is of even more importance, because the effects of cropping on undisturbed root-associated bacterial communities can be addressed. Here, we used a community prediction approach to describe the diversity of the root nodule bacterial communities of rooibos (Aspalathus linearis), an endemic legume crop from South Africa. The goal was to reveal whether patterns of root nodule community composition in paired cultivated and wild rooibos populations could be related to geographical distance, plant traits, and plant population type (i.e. cultivated or uncultivated). We identified a core of dominant and widespread Mesorhizobium ZOTUs that each defined one of 4 different root nodule community classes. Rooibos cultivation impacted root nodule bacterial diversity at regional and local scales, while the geographical origin of the root nodule communities was the strongest predictor of root nodule community structure. Beyond impacts of cultivation on root nodule bacterial diversity, this study suggests a mixture of dispersal limitation and ecological drift regionally, and selection by different plant populations locally, define the biogeography of rooibos root nodule bacterial communities.

ecology↗

Coalescence of rhizobial communities in soil interacts with fertilization and determines the assembly of rhizobia in root nodules

Soil microbial community coalescence, whereby entire microbial communities mix and compete in a new environmental setting, is a widespread phenomenon whose applicability for targeted root microbiome assembly has not been studied. Using a legume shrub adapted to nutrient poor soil, we tested for the first time how the assembly of communities of rhizobial root nodule symbionts is affected by the interaction of coalescence and fertilization. Seedlings of the rooibos [Aspalathus linearis (Burm.f.) Dahlg.], were raised in pairwise mixtures of soil from cultivated and uncultivated land of five farms, as well as the individual mixture components. A fragment of the symbiosis maker gene, nodA, was sequenced to characterize the taxonomic turnover of the rhizobia associated with all root nodules at the age of eight month. Soil mixing promoted taxonomic turnover in the rhizobial communities, while fertilization amplified such turnover by increasing the number of rhizobia that became more abundant after soil mixing. Soil mixing and fertilization had a synergistic effect on the abundance of a particular taxon, which was rare in the component soils but became highly abundant in fertilized plants raised in soil mixtures. These findings provide the first evidence that fertilizer addition can interact with soil microbial community coalescence, probably through increasing the chances for rare strains to prioritize root nodule colonization. The combination of soil mixing and fertilizer addition may be a still unexplored measure to (re)introduce root microbial mutualists in arable land.

ecology↗

Different ecological processes drive the assembly of dominant and rare root-associated bacteria in a promiscuous legume

Understanding how plant-associated microbial communities assemble and the roles they play in plant performance are major goals in microbial ecology. For nitrogen-fixing rhizobia, assemblages are mostly determined by filtering by the host as well as abiotic soil conditions. However, for legumes adapted to highly variable environments and nutrient-poor soils, filtering out rhizobial partners may not be an effective strategy to ensure symbiotic benefits. As a consequence, this can lead to net increases in rhizobial diversity driven by stochastic (neutral) assembly processes. Here, we addressed whether symbiotic promiscuity of rooibos (Aspalathus linearis Burm. Dahlgren), reflects increases in rhizobial diversity that are independent of the environmental conditions, following a neutral assembly. We performed a common garden experiment to assess whether root system size and location- and habitat-specific rhizobial propagule pools of rooibos affected rhizobial community diversity and composition. We found a dominance of drift in driving taxonomic turnover in the root nodule communities, but operating at different scales in the dominant Mesorhizobium symbionts and the rest of bacterial taxa. Specifically, drift triggered differentiation between the core rhizobial symbionts of rooibos due to dispersal limitation on a regional scale, whereas it dominated the assembly of non-dominant rhizobial taxa at the root level. This suggests the existence of a significant neutral component in rhizobial community assembly when selectivity by the host plant is low. We conclude that in this promiscuous legume neutral processes govern bacterial community root nodule community assembly, but that these operate at different scales in dominant and rare rhizobial symbionts of the plant.

ecology↗