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Kembel, S. W.

Publications and source records attributed to Kembel, S. W..

15 recordsLinked to original sources

Priority effects influence bacterial community assembly on temperate deciduous tree leaves

Microbial community assembly on leaves (the phyllosphere) is influenced by deterministic, stochastic, and historical processes. However, the importance of historical processes such as priority effects, where the timing and order of colonization influence community assembly, has not been extensively investigated in field-based phyllosphere studies. We designed a field experiment in a temperate forest in Quebec where we inoculated five strains of Methylobacterium onto the leaves of red maple and American beech trees, either early or late during the growing season. We quantified microbial community structure throughout the season using metabarcoding of a Methylobacterium-targeting rpoB primer as well as a 16S rRNA primer targeting the entire bacterial community. We show that the effects of inoculation on bacterial communities depend on inoculation timing: early-season inoculation led to strain-specific shifts in community composition, while late-season inoculation had no significant effect. Although the effect of early-season inoculation weakened over time, early- and late-season inoculation still led to different community compositions at the end of the growing season. Our study demonstrates that priority effects contribute to the assembly of phyllosphere bacterial communities under field conditions, with arrival timing and strain identity shaping community trajectories. Considering historical processes will thus be crucial for successful microbiome management.

ecology↗

Metapangenomics reveals host-driven adaptations of Methylobacterium to the phyllosphere

Bacteria inhabiting leaf surfaces - the phyllosphere - are crucial to plant health and ecosystem functioning. Methylobacterium is a taxonomically diverse, growth-promoting genus, ubiquitous on leaves. Different plant species host distinct Methylobacterium communities, but the genomic and functional basis of Methylobacterium symbiotic associations with particular host species remains poorly understood. Here, we used a metapangenomic approach to quantify the influence of host species on Methylobacterium assemblages, to identify genes potentially involved in Methylobacterium adaptations to host species, and to evaluate the contribution of Methylobacteriums accessory pangenome to these adaptations. We sequenced the metagenomes of 25 phyllosphere communities spanning five host species in a temperate forest in Quebec, Canada, and mapped these metagenomes onto Methylobacteriums pangenome to obtain nucleotide-level coverage and composition for each population on each individual host. We revealed strong divergences in the species- and gene-level community structure of Methylobacterium, driven by host phylogeny and plant form. Conifer communities were notably enriched in genes involved in amino acid, lipid, and carbohydrate metabolism; broadleaves, in genes involved in cell membrane, signalling, defense, and chemotaxis; and trees, in genes related to photosynthesis, oxidative phosphorylation, and translation. The shrub Corylus cornuta was a reservoir of Methylobacterium taxonomic diversity, and harboured numerous accessory genes under positive selection. Methylobacteriums accessory pangenome, evolving under weaker purifying selection, contributed importantly to gene-host associations, supporting its adaptive role. By linking genes to phyllosphere niches, our study shed light on the genetic basis of host adaptation and highlighted the crucial role of forest biodiversity in shaping microbial ecology and evolution.

ecology↗

Season and city shape urban bioaerosol composition beyond vegetation and socioeconomic gradients

Urban vegetation varies with socio-economic gradients, as lower-income neighborhoods often host sparser and less diverse green spaces. This disparity may affect respiratory health by influencing exposure to bioaerosols. Understanding the characteristics of this aerobiome could help anticipate risks related to allergies and other respiratory conditions. Here, we hypothesized that urban vegetation cover and socio-economic status shape urban bioaerosols. We sampled bioaerosols at 65 sites across three Canadian cities of varying population size and density using an active air sampler over four months, and characterized their bacterial, fungal, and pollen composition using amplicon sequencing. Seasonal alpha diversity varied significantly for fungi and pollen. Based on beta diversity, sampling period alone explained up to 40% of pollen, 29% of fungal, and 11% of bacterial community composition variation. In contrast, vegetation cover explained only a minor portion of the variance in bioaerosol composition, and median household income, almost none. These findings provide a critical baseline for understanding the urban aerobiome and highlight the need to study how vegetation identity and diversity, rather than cover alone, may shape bioaerosol dynamics in cities. As cities grow and urban greening initiatives expand, demystifying the aerobiome dynamics becomes an urgent public health priority.

microbiology↗

A phylogenomic and metagenomic meta-analysis of bacterial diversity in the phyllosphere lifts a veil on Hyphomicrobiales dark matter

The phyllosphere, or above-ground part of plants, hosts diverse bacterial communities that play critical ecological roles and provide beneficial functions for the plant. The Hyphomicrobiales (Alphaproteobacteria) are a highly diverse and ecologically important clade known to be key members of the plant microbiome, in particular in association with plant roots, but their diversity remain largely uncharacterized in the phyllosphere. Using a meta-analysis combining metabarcoding, metagenomics and phylogenomics, we explored the worldwide diversity of leaf-associated Hyphomicrobiales. We confirmed Methylobacterium was ubiquitous in the phyllosphere and revealed the dominance of two under-characterized Hyphomicrobiales taxa: Lichenibacterium, a lichen-associated genus previously identified as "1174-901-12" in taxonomic databases, and RH-AL1, an undescribed lineage of bacteria related to Beijerinckiaceae, previously isolated from coal slag. Despite their abundance in the phyllosphere, Lichenibacterium and RH_AL1 could not be properly detected by 16S rRNA gene barcoding, due in part to limitations of taxonomic resolution of the 16S rRNA gene and of representativeness in existing taxonomic databases, underlining limitations of this approach for their accurate identification in the phyllosphere. As for Methylobacterium, a significant proportion of Lichenibacterium and RH-AL1 were also detected in association with lichens and in environments with harsh conditions like exposed surfaces, air and snow, suggesting airborne or waterborne dispersal and high resilience in harsh environments. Overall, our study stresses the need to move toward metagenomics and culturomics to increase the representativeness of leaf-associated bacterial taxa in reference databases, and to improve our understanding of the evolutionary and functional mechanisms underpinning bacteria adaptations to living on plants. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=116 SRC="FIGDIR/small/671110v4_ufig1.gif" ALT="Figure 1"> View larger version (48K): org.highwire.dtl.DTLVardef@938d34org.highwire.dtl.DTLVardef@11b6df0org.highwire.dtl.DTLVardef@1ced858org.highwire.dtl.DTLVardef@dd7a55_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIGlobal meta-analysis reveals core Hyphomicrobiales in the phyllosphere C_LIO_LILichenibacterium and Methylobacterium dominate the phyllosphere and exposed surfaces C_LIO_LINovel phyllosphere clades RH-AL1 and JAJXWB01 were identified by phylogenomics C_LIO_LI16S rRNA gene limits taxonomic resolution in the phyllosphere; metagenomics refines taxonomy C_LI

microbiology↗

Richness and composition of phyllosphere Methylobacterium communities cause variation in Arabidopsis thaliana growth

The phyllosphere - the aerial parts of plants - forms a vast microbial habitat that harbors diverse bacterial communities playing key roles in ecosystem function. The foliar surface is thus a promising study system to investigate biodiversity-ecosystem function relationships. Researchers have found a positive correlation between leaf bacterial diversity and ecosystem productivity, but the causality of this relationship has yet to be demonstrated. To understand how the diversity and composition of phyllosphere bacterial communities could cause variation in the growth of their host plants, we assembled synthetic communities composed of different diversity and compositions of Methylobacterium strains - a plant growth-promoting bacterial genus ubiquitous in the phyllosphere - that we inoculated on Arabidopsis thaliana grown in gnotobiotic conditions. We hypothesized that (1) increasing Methylobacterium diversity should cause an increase in host growth; (2) strains should differ in their impact on host growth; and (3) the relationship between bacterial diversity and plant productivity should be strain-dependent. Our results supported our three hypotheses but revealed unpredicted patterns in how A. thaliana leaf biomass varied according to inoculated Methylobacterium strain richness and identity. Increasing bacterial richness induced a higher host leaf biomass, but only after an initial reduction in biomass, suggesting competition alleviation by multispecies interactions. Two Methylobacterium strains showed beneficial effects on A. thaliana growth, and one strain was detrimental for the plant. Community composition shaped the relationship between diversity and productivity, highlighting the importance of community mutualistic and antagonistic interactions. Furthermore, niche complementarity was likely the main ecological mechanism driving the diversity-productivity relationship in our study system. By demonstrating the causal effects of Methylobacterium community diversity and composition on host plant growth, our experiment shed light on the importance of phyllosphere bacteria in terrestrial ecosystem functioning.

ecology↗

Modeling plant-microbe interactions with species distribution models

Plants interact with diverse microorganisms that play a crucial role in plant growth and development. The diversity and distribution of plant microbiota are altered by anthropogenic environmental change, leading to subsequent impacts on ecosystems. Modeling the distribution of plant-associated microbes is critical for predicting and managing future changes in microbial function, but there remain challenges and open questions when developing these models. We present a conceptual framework for process-oriented predictive modeling of the distribution of plant-associated microbiota. We first describe different approaches to incorporating host plants into modeling microbial distributions, namely by including them as static variables, nesting them within microbial distribution models or incorporating them simultaneously via joint species distribution models. Additionally, we discuss issues associated with collecting and analyzing sequencing-based microbial data, emphasizing the importance of data normalization and careful interpretation of species distribution models. We further discuss how to incorporate evolutionary history into microbial distribution modeling. Finally, we present a case study demonstrating how incorporating host information can improve the prediction of microbial distributions. This study provides insights for predicting future distributions of plant-associated microbes under climate change and plant species redistribution, which can be generalized to other host-associated microbial systems.

ecology↗

Data-driven identification of major axes of functional variation in bacteria

The discovery of major axes of correlated functional variation among species and habitats has revealed the fundamental trade-offs structuring both functional and taxonomic diversity in eukaryotes such as plants. Whether such functional axes exist in the bacterial realm and whether they could explain bacterial taxonomic turnover among ecosystems remains unknown. Here we use a data-driven approach to leverage global genomic and metagenomic datasets to reveal the existence of major axes of functional variation explaining both evolutionary differentiation within Bacteria and their ecological sorting across diverse habitats. We show that metagenomic variation among bacterial communities from various ecosystems is structured along a few axes of correlated functional pathways. Similar clusters of traits explained phylogenetic trait variation among >16,000 bacterial genomes, suggesting that functional turnover among bacterial communities from distinct habitats does not only result from the differential filtering of similar functions among communities, but also from phylogenetic correlations among these functions. Concordantly, functional pathways associated with trait clusters that were most important for defining functional turnover among bacterial communities were also those that had the highest phylogenetic signal in the bacterial genomic phylogeny. This study overall underlines the important role of evolutionary history in shaping contemporary distributions of bacteria across ecosystems. Originality-Significance StatementIn this article, we use a trait screening approach based on genomic and metagenomic data to identify the key functional strategies of bacteria across ecosystems but also across the bacterial tree of life. This novel approach allows us to quantify the role of evolutionary processes in structuring microbial ecological differences among ecosystems. By reducing the high-dimensionality of trait variation observed among microorganisms around a small number of fundamental axes of trait covariation, we make a significant step towards generalization of the drivers of biological diversity in microbes but also across study systems. This research provide a major advance in our understanding of the origin and maintenance of bacterial biological diversity, expanding on related findings for plants and animals.

ecology↗

Diversity and biogeography of plant leaf bacteria along a latitudinal gradient

Plant-associated microbes are essential for promoting plant well-being, maintaining biodiversity, and supporting ecosystem function. However, little is known about the geographic distribution of plant-microbe symbioses and how they are formed and change along latitudinal gradients. Here we identified leaf bacteria for 328 plant species sampled from 10 forests along a tropical to temperate gradient in China. We analyzed the diversity and composition of plant leaf-associated bacteria and quantified the contributions of hosts, habitats, and neighborhood plants to the plant-bacterial symbiosis. We found a strong latitudinal gradient in leaf bacterial diversity and composition. Bacterial assemblages on leaves were most strongly selected by host plants, and the selection pressure increased with latitude. In contrast, at low latitudes and at large geographical scales multiple factors were found to jointly regulate bacterial community composition. Our result also showed that plant-bacteria symbiotic networks were structured by network hub bacteria taxa with high co-occurrence network centrality, and the abundance of temperate hub taxa was more influenced by host plants than that in tropical forests. For the first time, we documented a previously unrecognized latitudinal gradient in plant-bacterial symbioses that was regulated by a joint effect of multiple factors at low latitudes but mostly by host selection at high latitudes, implying that leaf microbiomes are likely to respond differently to global change along the latitudinal gradient.

ecology↗

Comprehensive phylogenomics of Methylobacterium reveals four evolutionary distinct groups and underappreciated phyllosphere diversity.

Methylobacterium is a group of methylotrophic microbes associated with soil, fresh water, and particularly the phyllosphere, the aerial part of plants that has been well-studied in terms of physiology but whose evolutionary history and taxonomy are unclear. Recent work has suggested that Methylobacterium is much more diverse than thought previously, questioning its status as an ecologically and phylogenetically coherent taxonomic genus. However, taxonomic and evolutionary studies of Methylobacterium have mostly been restricted to model species, often isolated from habitats other than the phyllosphere, and have yet to utilize comprehensive phylogenomic methods to examine gene trees, gene content, or synteny. By analyzing 189 Methylobacterium genomes from a wide range of habitats, including the phyllosphere, we inferred a robust phylogenetic tree while explicitly accounting for the impact of horizontal gene transfers. We showed that Methylobacterium contains four evolutionary distinct groups of bacteria (namely A, B, C, D), characterized by different genome size, GC content, gene content and genome architecture, revealing the dynamic nature of Methylobacterium genomes. In addition of recovering 59 described species, we identified 45 candidate species, mostly phyllosphere-associated, stressing the significance of plants as a reservoir of Methylobacterium diversity. We inferred an ancient transition from a free-living lifestyle to association with plant roots in Methylobacteriaceae ancestor, followed by phyllosphere association of three of the major groups (A, B, D), which early branching in Methylobacterium history was heavily obscured by HGT. Together, our work lays the foundations for a thorough redefinition of Methylobacterium taxonomy, beginning with the abandon of Methylorubrum.

genomics↗

Dominance of coniferous and broadleaved trees drives bacterial associations with boreal feather mosses

The composition of ecologically important moss-associated bacterial communities seems to be mainly driven by host species, but may also be shaped by environmental conditions related with tree-canopy dominance. The moss phyllosphere has been studied in coniferous forests while broadleaf forests remain understudied. To determine if host species or environmental conditions defined by tree-canopy dominance drives the bacterial diversity in the moss phyllosphere, we used 16S rRNA gene amplicon sequencing to quantify changes in bacterial communities as a function of host species (Pleurozium schreberi and Ptilium crista-castrensis) and forest type (coniferous black spruce versus deciduous broadleaf trembling aspen) in eastern Canada. Forest type, not host species, was the main factor affecting moss phyllosphere bacterial community composition, though the interaction of both variables was significant. Bacterial -diversity was highest in spruce forests, while there was greater turnover ({beta}- diversity) and higher {gamma}-diversity in aspen forests. Unexpectedly, Cyanobacteria were much more relatively abundant in aspen than in spruce forests, with the bacterial family Nostocaceae (Cyanobacteria) differing the most between both forest types. Our results suggest that the increasing change in dominance from coniferous to broadleaf trees due to natural and anthropic disturbances is likely to affect the composition of moss-associated bacteria in boreal forests.

microbiology↗

FINE-SCALE ADAPTATIONS TO ENVIRONMENTAL VARIATION AND GROWTH STRATEGIES DRIVE PHYLLOSPHERE METHYLOBACTERIUM DIVERSITY.

Methylobacterium is a prevalent bacterial genus of the phyllosphere. Despite its ubiquity, little is known about the extent to which its diversity reflects neutral processes like migration and drift, versus environmental filtering of life history strategies and adaptations. In two temperate forests, we investigated how phylogenetic diversity within Methylobacterium was structured by biogeography, seasonality, and growth strategies. Using deep, culture-independent barcoded marker gene sequencing coupled with culture-based approaches, we uncovered a considerable diversity of Methylobacterium in the phyllosphere. We cultured different subsets of Methylobacterium lineages depending upon the temperature of isolation and growth (20 {degrees}C or 30 {degrees}C), suggesting long-term adaptation to temperature. To a lesser extent than temperature adaptation, Methylobacterium diversity was also structured across large (>100km; between forests) and small geographical scales (<1.2km within forests), among host tree species, and was dynamic over seasons. By measuring growth of 79 isolates at different temperature treatments, we observed contrasting growth performances, with strong lineage- and season-dependent variations in growth strategies. Finally, we documented a progressive replacement of lineages with a high-yield growth strategy typical of cooperative, structured communities, in favor of those characterized by rapid growth, resulting in convergence and homogenization of community structure at the end of the growing season. Together our results show how Methylobacterium is phylogenetically structured into lineages with distinct growth strategies, which helps explain their differential abundance across regions, host tree species, and time. This works paves the way for further investigation of adaptive strategies and traits within a ubiquitous phyllosphere genus. ImportanceMethylobacterium is a bacterial group tied to plants. Despite its ubiquity and importance to their hosts, little is known about the processes driving Methylobacterium community dynamics. By combining traditional culture-dependent and independent (metabarcoding) approaches, we monitored Methylobacterium diversity in two temperate forests over a growing season. On the surface of tree leaves, we discovered remarkably diverse and dynamic Methylobacterium communities over short temporal (from June to October) and spatial scales (within 1.2 km). Because we cultured different subsets of Methylobacterium diversity depending on the temperature of incubation, we suspected that these dynamics partly reflected climatic adaptation. By culturing strains in lab conditions mimicking seasonal variations, we found that diversity and environmental variations were indeed good predictors of Methylobacterium growth performances. Our findings suggest that Methylobacterium community dynamics at the surface of tree leaves results from the succession of strains with contrasted growth strategies in response to environmental variations.

microbiology↗

Links between mouse and vole social networks and their gut microbiomes support predictions from metacommunity theory

Metacommunity theory predicts that strongly connected individuals will harbour similar gut microbiomes (GMs) and affiliating with more individuals should increase GM diversity. Additionally, cross-species bacterial transmission may play a role in how interspecific interactions affect host community dynamics. We tracked sympatric mice (Peromyscus maniculatus) and voles (Myodes gapperi) and constructed social networks for each species and both species together. We tested whether: 1) similarity in GM composition between individuals correlates with their social proximity within and across species; 2) GM diversity correlates with a hosts number of conspecific or heterospecific neighbours. We could not differentiate associations between GM composition and mouse social proximity or habitat. In voles, social proximity explained part of the GM composition. GM composition associated with interspecific social proximity, and mouse GM diversity correlated with number of vole neighbours. Contributions of host-host bacterial transmission to the GM partly follow metacommunity theory but depend on host species.

ecology↗

Gut microbiome modulates behaviour and life history in two wild rodents

Laboratory studies demonstrate that the gut microbiome can regulate host anxiety and exploratory behaviour. While this has implications for human health, it could have ecological and evolutionary implications for wild populations, a hitherto untested hypothesis. We tested whether the microbiome can directly modulate host behaviour and thereby affect life history in wild mice (Peromyscus maniculatus) and voles (Myodes gapperi). We compared the microbiome composition, exploration and anxiety behaviours, and home range of mice and voles before and after chronic antibiotic treatment and measured survival during treatment. Treated animals had lower diversity and relative abundance of most bacterial phyla save for Proteobacteria which increased in relative abundance. In mice, antibiotic treatment increased exploration and decreased home range without impacting survival. In voles, it lowered survival such that we could not test its effect on behaviour. Therefore, the microbiome can directly impact behaviour and host life history in the wild.

ecology↗

Drivers of phyllosphere microbial functional diversity in a neotropical forest

BackgroundThe phyllosphere is an important microbial habitat but our understanding of how plant hosts drive the composition of their associated leaf microbial communities and whether taxonomic associations between plants and phyllosphere microbes represent adaptive matching remains limited. In this study we quantify bacterial functional diversity in the phyllosphere of 17 tree species in a diverse neotropical forest using metagenomic shotgun sequencing. We ask how hosts drive the functional composition of phyllosphere communities and their turnover across tree species, using host functional traits and phylogeny. We compare functional predictions inferred from 16S gene sequencing with functions estimated from metagenomic shotgun sequencing. ResultsNeotropical tree phyllosphere communities are dominated by functions related to the metabolism of carbohydrates, amino acids and energy acquisition, along with environmental signalling pathways involved in membrane transport. While most functional variation was observed within communities, there is non-random assembly of microbial functions across host species possessing different leaf traits. Metabolic functions related to biosynthesis and degradation of secondary compounds, along with signal transduction and cell-cell adhesion were particularly important in driving the match between microbial functions and host traits. These microbial functions were also evolutionarily conserved across the host phylogeny. Functional predictions inferred from 16S gene sequences were weakly correlated with functional annotations from the same samples through metagenomic shotgun sequencing, especially for finer-scale functional annotations. ConclusionsFunctional profiling based on metagenomic shotgun sequencing offers evidence for the presence of a core functional microbiome across phyllosphere communities of neotropical trees. While functional turnover across phyllosphere communities is relatively small, the association between microbial functions and leaf trait gradients among host species supports a significant role for plant hosts as selective filters on phyllosphere community assembly. This interpretation is supported by the presence of phylogenetic signal for the microbial traits driving inter-community variation across the host phylogeny. Our comparison of functional annotations derived from 16S genes versus metagenomic shotgun sequencing suggests caution in using functions inferred from 16S genes for studying ecological dynamics in phyllosphere communities. Taken together, our results suggest that there is adaptive matching between phyllosphere microbes and their plant hosts.

ecology↗

Ecophylogenetics Reveals the Evolutionary Associations between Mammals and their Gut Microbiota

A tantalizing hypothesis posits that mammals coevolved with their gut microbiota. Unfortunately, the limited resolution of microbial taxonomy hinders the exploration of this hypothesis and specifically challenges the discovery of gut microbes that are linked to mammalian evolution. To address this, we developed a novel approach that groups microbes into new, more meaningful taxonomic units based on their common ancestry and ecological redundancy. Treating mammalian lineages as different ecosystems, we quantified the distribution of these microbial taxa across mammals. Our analysis discovered monophyletic clades of gut bacteria that are unexpectedly prevalent, or conserved, across all mammals, as well as conserved clades that are exclusive to particular mammalian lineages. These clades often manifest phylogenetic patterns indicating that they are subject to selection. Lineage - specific changes in clade conservation, including a human-accelerated loss of conserved clades, suggest that mammalian evolution associates with a change in the selective regimes that act on gut microbiota. Collectively, these results point to the existence of microbes that possess traits that facilitate their dispersion or survival in the mammalian gut, possibly because they are subject to host selection. Ultimately, our analysis clarifies the relationship between the diversification of the gut microbiome and mammalian evolutionary history.

microbiology↗