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Organic carbon availability in soil is crucial for shaping microbial communities, yet, uncertainties persist concerning microbial adaptations to carbon levels and the ensuing ecological and evolutionary consequences. We investigated organic carbon metabolism, antibiotic resistance, and virus-host interactions in soils subjected to 40 y of chemical and organic fertilization that led to contrasting carbon availability: carbon-poor and carbon-rich soils, respectively. Carbon-poor soils drove the enrichment of putative genes involved in organic matter decomposition and exhibited specialization in utilizing complex organic compounds, reflecting scramble competition. This specialization confers a competitive advantage of microbial communities in carbon-poor soils but reduces their buffering capacity in terms of organic carbon metabolisms, making them more vulnerable to environmental fluctuations. Additionally, in carbon-poor soils, viral auxiliary metabolic genes linked to organic carbon metabolism increased host competitiveness and environmental adaptability through a strategy akin to "piggyback the winner." Furthermore, putative antibiotic resistance genes, particularly in low-abundance drug categories, were enriched in carbon-poor soils as an evolutionary consequence of chemical warfare (i.e., interference competition). This raises concerns about the potential dissemination of antibiotic resistance from conventional agriculture that relies on chemical-only fertilization. Consequently, carbon starvation resulting from long-term chemical-only fertilization increases microbial adaptations to competition, underscoring the importance of implementing sustainable agricultural practices to mitigate the emergence and spread of antimicrobial resistance and to increase soil carbon storage.
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Carbono , Solo , Solo/química , Carbono/metabolismo , Agricultura/métodos , Antibacterianos/farmacologia , Farmacorresistência Bacteriana , Microbiologia do SoloRESUMO
Ecological corridors promote species coexistence in fragmented habitats where dispersal limits species fluxes. The corridor concept was developed and investigated with macroorganisms in mind, while microorganisms, the invisible majority of biodiversity, were disregarded. We analyzed the effect of corridors on the dynamics of endospheric fungal assemblages associated with plant roots at the scale of 1 m over 2 years (i.e. at five time points) by combining an experimental corridor-mesocosm with high-throughput amplicon sequencing. We showed that plant root endospheric mycobiota were sensitive to corridor effects when the corridors were set up at a small spatial scale. The endospheric mycobiota of connected plants had higher species richness, lower beta-diversity, and more deterministic assembly than the mycobiota of isolated plants. These effects became more pronounced with the development of host plants. Biotic corridors composed of host plants may thus play a key role in the spatial dynamics of microbial communities and may influence microbial diversity and related ecological functions.
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Ecossistema , Microbiota , Biodiversidade , Plantas , Raízes de Plantas/microbiologiaRESUMO
Rare species are crucial components of the highly diverse soil microbial pool and over-proportionally contribute to the soil functions. However, much remains unknown about their assembling rules. The biogeographic patterns and species aggregations of the rare bacterial biosphere were assessed using 140 soil samples from a gradient of 2000 km across the main tea-producing areas in China. About 96% OTUs with ~40% sequences were classified as rare taxa. The rare bacterial communities were significantly affected by geographical regions and showed distance-decay effects, indicating that the rare bacteria are not cosmopolitan, they displayed a pattern of limited dispersal and were restricted to certain sites. Variation partitioning analysis (VPA) revealed that environmental variation and spatial factors explained 12.5% and 6.4%, respectively, of the variance in rare bacterial community. The Mantel and partial Mantel tests also showed that the environmental factors had stronger (~3 times) impacts than spatial factors. The null model showed that deterministic processes contributed more than stochastic processes in rare bacterial assembly (75% vs. 25%). There is likely an enrichment in ecological functions within the rare biosphere, considering this high contribution of deterministic processes in the assembly. In addition, the assembly of rare taxa was found to be mainly driven by soil pH. Overall, this study revealed that rare bacteria were not cosmopolitan, and their assembly was more driven by deterministic processes. These findings provided a new comprehensive understanding of rare bacterial biogeographic patterns and assembly rules.
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Microbiologia do Solo , Solo , Bactérias/genética , ChinaRESUMO
A host-plant and its associated microbiota depend on one another. However, the assembly process and the functioning of host-associated microbiota are poorly understood. Herein, rice was used as model plant to investigate the assemblage of bacterial microbiota, including those in the seed, root endosphere and rhizosphere. We also assessed the degree to which endosphere and rhizosphere communities were influenced by vertical transmission through seed and identified the core microbes that potentially associated with plant phenotypic properties. Plant microhabitat, rather than subspecies type, was the major driver shaping plant-associated bacterial microbiota. Deterministic processes were primarily responsible for community assembly in all microhabitats. The influence of vertical transmission from seed to root-associated bacterial communities appeared to be quite weak (endosphere) or even absent (rhizosphere). A core microbial community composed of 15 generalist species persisted across different microhabitats and represented key connectors in networks. Host-plant functional traits were linked to the relative abundance of these generalist core microbes and could be predicted from them using machine learning algorithms. Overall, bacterial microbiota is assembled by host-plant interactions in a deterministic-based manner. This study enhances our understanding of the driving mechanisms and associations of microbiota in various plant microhabitats and provides new perspectives to improve plant performance.
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Microbiota , Oryza , Raízes de Plantas , Rizosfera , Sementes , Microbiologia do SoloRESUMO
Fungal communities in the root endosphere are heterogeneous at fine scale. The passenger hypothesis assumes that this heterogeneity is driven by host plant distribution. Plant composition and host plant configuration should then influence root fungal assemblages. We used a large-scale experimental design of 25 mixtures of grassland plants. We sampled Brachypodium pinnatum in each mesocosm, and used amplicon mass-sequencing to analyze the endospheric mycobiota. We used plant distribution maps to assess plant species richness and evenness (heterogeneity of composition), and patch size and the degree of isolation of B. pinnatum (heterogeneity of configuration) on fungal community assembly. The Glomeromycotina community in B. pinnatum roots was not related to either floristic heterogeneity or productivity. For Ascomycota, the composition of operational taxonomic units (OTUs) was driven by plant evenness while OTU richness decreased with plant richness. For Basidiomycota, richness increased with host plant aggregation and connectivity. Plant productivity influenced Ascomycota, inducing a shift in OTU composition and decreasing evenness. Plant heterogeneity modified root mycobiota, with potential direct (i.e. host preference) and indirect (i.e. adaptations to abiotic conditions driven by plant occurrence over time) effects. Plant communities can be envisioned as microlandscapes consisting of a variety of fungal niches.
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Ascomicetos/classificação , Basidiomycota/classificação , Brachypodium/microbiologia , Glomeromycota/classificação , Raízes de Plantas/microbiologiaRESUMO
In the processes controlling ecosystem fertility, fungi are increasingly acknowledged as key drivers. However, our understanding of the rules behind fungal community assembly regarding the effect of soil fertility level remains limited. Using soil samples from typical tea plantations spanning c. 2167 km north-east to south-west across China, we investigated the assemblage complexity and assembly processes of 140 fungal communities along a soil fertility gradient. The community dissimilarities of total fungi and fungal functional guilds increased with increasing soil fertility index dissimilarity. The symbiotrophs were more sensitive to variations in soil fertility compared with pathotrophs and saprotrophs. Fungal networks were larger and showed higher connectivity as well as greater potential for inter-module connection in more fertile soils. Environmental factors had a slightly greater influence on fungal community composition than spatial factors. Species abundance fitted the Zipf-Mandelbrot distribution (niche-based mechanisms), which provided evidence for deterministic-based processes. Overall, the soil fungal communities in tea plantations responded in a deterministic manner to soil fertility, with high fertility correlated with complex fungal community assemblages. This study provides new insights that might contribute to predictions of fungal community complexity.
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Ecossistema , Fungos , Solo , China , Microbiologia do SoloRESUMO
Plants can no longer be considered as standalone entities and a more holistic perception is needed. Indeed, plants harbor a wide diversity of microorganisms both inside and outside their tissues, in the endosphere and ectosphere, respectively. These microorganisms, which mostly belong to Bacteria and Fungi, are involved in major functions such as plant nutrition and plant resistance to biotic and abiotic stresses. Hence, the microbiota impact plant growth and survival, two key components of fitness. Plant fitness is therefore a consequence of the plant per se and its microbiota, which collectively form a holobiont. Complementary to the reductionist perception of evolutionary pressures acting on plant or symbiotic compartments, the plant holobiont concept requires a novel perception of evolution. The interlinkages between the plant holobiont components are explored here in the light of current ecological and evolutionary theories. Microbiome complexity and the rules of microbiotic community assemblage are not yet fully understood. It is suggested that the plant can modulate its microbiota to dynamically adjust to its environment. To better understand the level of plant dependence on the microbiotic components, the core microbiota need to be determined at different hierarchical scales of ecology while pan-microbiome analyses would improve characterization of the functions displayed.
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Microbiota , Plantas/microbiologia , Evolução BiológicaRESUMO
A key objective in ecology is to understand how cooperative strategies evolve and are maintained in species networks. Here, we focus on the tri-trophic relationship between arbuscular mycorrhizal (AM) fungi, host plants, and fungivores to ask if host plants are able to protect their mutualistic mycorrhizal partners from being grazed. Specifically, we test whether secondary metabolites are transferred from hosts to fungal partners to increase their defense against fungivores. We grew Plantago lanceolata hosts with and without mycorrhizal inoculum, and in the presence or absence of fungivorous springtails. We then measured fungivore effects on host biomass and mycorrhizal abundance (using quantitative PCR) in roots and soil. We used high-performance liquid chromatography to measure host metabolites in roots, shoots, and hyphae, focusing on catalpol, aucubin, and verbascoside. Our most striking result was that the metabolite catalpol was consistently found in AM fungal hyphae in host plants exposed to fungivores. When fungivores were absent, catalpol was undetectable in hyphae. Our results highlight the potential for plant-mediated protection of the mycorrhizal hyphal network.
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Comportamento Alimentar/fisiologia , Hifas/metabolismo , Insetos/fisiologia , Micorrizas/fisiologia , Plantago/metabolismo , Plantago/microbiologia , Animais , SimbioseRESUMO
Microorganisms are associated with all plants, recently leading to the hologenome concept. We reviewed the assembly processes of plant microbiota and analyzed its structure during the emergence of dysbioses. In particular, we discussed the Anna Karenina Principle (AKP) based on Leo Tolstoy's assertion applied to plant microbiota: 'All healthy microbiota are alike; each disease-associated microbiota is sick in its own way.' We propose the AKP to explain how stochastic processes in plant microbiota assembly due to several external stressors could lead to plant diseases. Finally, we propose the AKP to conceptualize plant dysbioses as a transitory loss of host capacity to regulate its microbiota, implying a loss of function that leads to a reduction of the host's fitness.
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Disbiose , Microbiota , PlantasRESUMO
The use of stable-isotope probing (SIP) allows tracing specific labeled substrates into fungi leading to a better understanding of their role in biogeochemical cycles and their relationship with their environment. Stable isotope probing combined with ribosomal RNA molecule, conserved in the three kingdoms of life, and messenger RNA analysis permits the linkage of diversity and function. Here, we describe two methods designed to investigate the interactions between plants and their associated mycorrhizal compartment by tracing carbon flux from the host plant to its symbionts.
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Micorrizas , RNA , Marcação por Isótopo/métodos , Micorrizas/genética , Isótopos , RNA Ribossômico/genética , Plantas/genética , Plantas/microbiologia , Isótopos de CarbonoRESUMO
The hologenome concept considers the entity formed by a host and its microbiota, the holobiont, as new level of hierarchical organization subject to neutral and selective forces. We used grafted plants to formally evaluate the hologenome concept. We analyzed the root-endosphere microbiota of two independent watermelon and grapevine plant systems, including ungrafted and reciprocal-grafting combinations. Grafted and ungrafted hosts harbor markedly different microbiota compositions. Furthermore, the results indicate a non-random assembly of bacterial communities inhabiting the root endosphere of chimeric plants with interactive effect of both the rootstock and scion on the recruitment of microorganisms. Because chimeric plants did not have a random microbiota, the null hypothesis that holobionts assemble randomly and hologenome concept is an intellectual construction only can be rejected. The study supports the relevance of hologenome as biological level of organization and opens new avenues for a better fundamental understanding of plants as holobionts.
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BACKGROUND: Rice is the second most produced crop worldwide, but is highly susceptible to drought. Micro-organisms can potentially alleviate the effects of drought. The aim of the present study was to unravel the genetic factors involved in the rice-microbe interaction, and whether genetics play a role in rice drought tolerance. For this purpose, the composition of the root mycobiota was characterized in 296 rice accessions (Oryza sativa L. subsp. indica) under control and drought conditions. Genome wide association mapping (GWAS) resulted in the identification of ten significant (LOD > 4) single nucleotide polymorphisms (SNPs) associated with six root-associated fungi: Ceratosphaeria spp., Cladosporium spp., Boudiera spp., Chaetomium spp., and with a few fungi from the Rhizophydiales order. Four SNPs associated with fungi-mediated drought tolerance were also found. Genes located around those SNPs, such as a DEFENSIN-LIKE (DEFL) protein, EXOCYST TETHERING COMPLEX (EXO70), RAPID ALKALINIZATION FACTOR-LIKE (RALFL) protein, peroxidase and xylosyltransferase, have been shown to be involved in pathogen defense, abiotic stress responses and cell wall remodeling processes. Our study shows that rice genetics affects the recruitment of fungi, and that some fungi affect yield under drought. We identified candidate target genes for breeding to improve rice-fungal interactions and hence drought tolerance.
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BACKGROUND: From a theoretical ecology point of view, microbiomes are far more complex than expected. Besides competition and competitive exclusion, cooperative microbe-microbe interactions have to be carefully considered. Metabolic dependencies among microbes likely explain co-existence in microbiota. METHODOLOGY: In this in silico study, we explored genome-scale metabolic models (GEMs) of 193 bacteria isolated from Arabidopsis thaliana roots. We analyzed their predicted producible metabolites under simulated nutritional constraints including "root exudate-mimicking growth media" and assessed the potential of putative metabolic exchanges of by- and end-products to avoid those constraints. RESULTS: We found that the genome-encoded metabolic potential is quantitatively and qualitatively clustered by phylogeny, highlighting metabolic differentiation between taxonomic groups. Random, synthetic combinations of increasing numbers of strains (SynComs) indicated that the number of producible compounds by GEMs increased with average phylogenetic distance, but that most SynComs were centered around an optimal phylogenetic distance. Moreover, relatively small SynComs could reflect the capacity of the whole community due to metabolic redundancy. Inspection of 30 specific end-product metabolites (i.e., target metabolites: amino acids, vitamins, phytohormones) indicated that the majority of the strains had the genetic potential to produce almost all the targeted compounds. Their production was predicted (1) to depend on external nutritional constraints and (2) to be facilitated by nutritional constraints mimicking root exudates, suggesting nutrient availability and root exudates play a key role in determining the number of producible metabolites. An answer set programming solver enabled the identification of numerous combinations of strains predicted to depend on each other to produce these targeted compounds under severe nutritional constraints thus indicating a putative sub-community level of functional redundancy. CONCLUSIONS: This study predicts metabolic restrictions caused by available nutrients in the environment. By extension, it highlights the importance of the environment for niche potential, realization, partitioning, and overlap. Our results also suggest that metabolic dependencies and cooperation among root microbiota members compensate for environmental constraints and help maintain co-existence in complex microbial communities. Video Abstract.
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Proteínas de Arabidopsis , Arabidopsis , Microbiota , Filogenia , Ecologia , Microbiota/genética , Peptídeos e Proteínas de Sinalização IntracelularRESUMO
INTRODUCTION: Microbial generalists and specialists are thought to have distinct impacts on community dynamics, while there have been limited efforts to estimate their contribution to microbial diversity. OBJECTIVES: We aimed to resolve this research gap in microbial ecology to strengthen our understanding of the biogeography of microbial diversity, with implications for global-scale biodiversity mapping. METHODS: Herein, we identified the ecological characteristics of microbial generalists and specialists across over 3,000 farmland soil samples from eleven countries that encompassed seven climate types. RESULTS: Considering the distinct distributions of generalists and specialists in degree of connexions, betweenness and as key species in network topology, both generalists and specialists contributed to species interactions, though through different modalities. A stronger signature of deterministic processes in specialists indicated their lower tolerance to environment fluctuations. Generalists, in contrast, were more characterized by stochastic processes with higher diversification and transition rates that suggested more important roles in maintaining community stability when exposed to environmental disturbances. The relationship between latitude and diversity combining with distance-decay effects showed that generalists dampened microbial biogeographical patterns, with contrasting impacts by specialists. CONCLUSION: By demonstrating the ecological characteristics of microbial generalists and specialists, this study deepens our understanding of microbial diversity and highlights the need to impart systematic distinctions among different categories of species when modelling and predicting the fate of ecosystems in the face of global climate change, rather than assuming that species are functionally equivalent.
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Ecossistema , Solo , Bactérias , Fazendas , Microbiologia do SoloRESUMO
Agricultural intensification has been demonstrated to induce a loss of biodiversity. Despite the key role of symbiotic microorganisms in plant nutrition and protection, the impact of agricultural intensification on these microorganisms is not fully understood. Organic farming and field edges (as semi-natural elements) may promote a higher microbial diversity thanks to lower anthropic disturbance and higher plant diversity. We sampled wheat individuals in pairs of wheat fields (one organic and one conventional) along a distance gradient to the edges (hedgerow vs. grassy), in 20 landscape windows selected along an uncorrelated gradient of organic farming and hedgerow density. We demonstrated that organic farming shaped microbial composition and increased fungal and bacterial richness, while hedgerows had a neutral or negative effect on richness depending on the microbial phyla considered. In contrast to bacteria, fungal communities were heterogeneously distributed within fields, having a higher diversity for some phyla close to field edges. Overall we highlighted that fungi responded more to the field scale while bacteria were more affected by landscape scale. The effect of agricultural intensification on plant microbiota and therefore on the functions provided by microorganisms to the plants has to be considered at a multiple spatial scale-from field to landscape.
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Microbiota , Agricultura Orgânica , Agricultura , Biodiversidade , Ecossistema , Humanos , TriticumRESUMO
Understanding how microorganism-microorganism interactions shape microbial assemblages is a key to deciphering the evolution of dependencies and co-existence in complex microbiomes. Metabolic dependencies in cross-feeding exist in microbial communities and can at least partially determine microbial community composition. To parry the complexity and experimental limitations caused by the large number of possible interactions, new concepts from systems biology aim to decipher how the components of a system interact with each other. The idea that cross-feeding does impact microbiome assemblages has developed both theoretically and empirically, following a systems biology framework applied to microbial communities, formalized as microbial systems ecology (MSE) and relying on integrated-omics data. This framework merges cellular and community scales and offers new avenues to untangle microbial coexistence primarily by metabolic modeling, one of the main approaches used for mechanistic studies. In this mini-review, we first give a concise explanation of microbial cross-feeding. We then discuss how MSE can enable progress in microbial research. Finally, we provide an overview of a MSE framework mostly based on genome-scale metabolic-network reconstruction that combines top-down and bottom-up approaches to assess the molecular mechanisms of deterministic processes of microbial community assembly that is particularly suitable for use in synthetic biology and microbiome engineering.
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Modern plant breeding and agrosystems artificialization could have altered plants' ability to filter and recruit beneficial microorganisms in its microbiota. Thus, compared to modern cultivars, we hypothesized that root-endosphere microbiota in modern wheat cultivars are less resistant to colonization by fungi and bacteria and thus more susceptible to also recruit more pathogens. We used an in-field experimental design including six wheat varieties (three ancient vs. three modern) grown in monoculture and in mixture (three replicates each). Endospheric microbiota of wheat roots were analyzed on four individuals sampled randomly in each plot. Composition-based clustering of sequences was then characterized from amplicon mass-sequencing. We show that the bacterial and fungal microbiota composition in wheat roots differed between ancient and modern wheat cultivar categories. However, the responses observed varied with the group considered. Modern cultivars harbored higher richness of bacterial and fungal pathogens than ancient cultivars. Both cultivar types displayed specific indicator species. A synergistic effect was identified in mixtures of modern cultivars with a higher root endospheric mycobiota richness than expected from a null model. The present study shows the effect of plant breeding on the microbiota associated plant roots. The results call for making a diagnosis of the cultivar's endospheric-microbiota composition. These new results also suggest the importance of a holobiont-vision while considering plant selection in crops and call for better integration of symbiosis in the development of next-generation agricultural practices.
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Environmental genomics and genome-wide expression approaches deal with large-scale sequence-based information obtained from environmental samples, at organismal, population or community levels. To date, environmental genomics, transcriptomics and proteomics are arguably the most powerful approaches to discover completely novel ecological functions and to link organismal capabilities, organism-environment interactions, functional diversity, ecosystem processes, evolution and Earth history. Thus, environmental genomics is not merely a toolbox of new technologies but also a source of novel ecological concepts and hypotheses. By removing previous dichotomies between ecophysiology, population ecology, community ecology and ecosystem functioning, environmental genomics enables the integration of sequence-based information into higher ecological and evolutionary levels. However, environmental genomics, along with transcriptomics and proteomics, must involve pluridisciplinary research, such as new developments in bioinformatics, in order to integrate high-throughput molecular biology techniques into ecology. In this review, the validity of environmental genomics and post-genomics for studying ecosystem functioning is discussed in terms of major advances and expectations, as well as in terms of potential hurdles and limitations. Novel avenues for improving the use of these approaches to test theory-driven ecological hypotheses are also explored.
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Ecossistema , Meio Ambiente , Metagenômica , Animais , Biologia Computacional , Expressão Gênica , ProteômicaRESUMO
Evolution is generally considered to be unpredictable because genetic variations are known to occur randomly. However, remarkable patterns of repeated convergent evolution are observed, for instance, loss of pigments by organisms living in caves. Analogous phenotypes appear in similar environments, sometimes in response to similar constraints. Alongside randomness, a certain evolutionary determinism also exists, for instance, the selection of particular phenotypes subjected to particular environmental constraints in the "evolutionary funnel." We pursue the idea that eco-evolutionary specialization is in some way determinist. The conceptual framework of phenotypic changes entailing specialization presented in this essay explains how evolution can be predicted. We also discuss how the predictability of evolution could be tested using the case of metabolic specialization through gene losses. We also put forward that microorganisms could be key models to test and possibly make headway evolutionary predictions and knowledge about evolution.
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Microbes encompass tremendous biodiversity, provide support to all living forms, including humans, and play an important role in many ecosystem services. The rules that govern microorganism community assembly are increasingly revealed due to key advances in molecular and analytical methods but their understanding remain a key challenge in microbial ecology. The existence of biogeographic patterns within microbial communities has been established and explained in relation to landscape-scale processes, including selection, drift, dispersal and mutation. The effect of habitat patchiness on microorganisms' assembly rules remains though incompletely understood. Here, we review how landscape ecology principles can be adapted to explore new perspectives on the mechanisms that determine microbial community structure. To provide a general overview, we characterize microbial landscapes, the spatial and temporal scales of the mechanisms that drive microbial assembly and the feedback between microorganisms and landscape structure. We provide evidence for the effects of landscape heterogeneity, landscape fragmentation and landscape dynamics on microbial community structure, and show that predictions made for macro-organisms at least partly also apply to microorganisms. We explain why emerging metacommunity approaches in microbial ecology should include explicit characterization of landscape structure in their development and interpretation. We also explain how biotic interactions, such as competition, prey-predator or mutualist relations may influence the microbial landscape and may be involved in the above-mentioned feedback process. However, we argue that the application of landscape ecology to the microbial world cannot simply involve transposing existing theoretical frameworks. This is due to the particularity of these organisms, in terms of size, generation time, and for some of them, tight interaction with hosts. These characteristics imply dealing with unusual and dependent space and time scales of effect. Evolutionary processes have also a strong importance in microorganisms' response to their landscapes. Lastly, microorganisms' activity and distribution induce feedback effects on the landscape that have to be taken into account. The transposition of the landscape ecology framework to microorganisms provides many challenging research directions for microbial ecology.