Diversity recruits resilience via metabolite signaling.

The microbiomes of host organisms and their direct source environments are closely linked and key for shaping microbial community dynamics. The relationship between these linked dynamics is largely unexplored because source substrates are usually unavailable. To address this current knowledge gap, we employed bacteriovorous Caenorhabditis nematodes as a unique model system, for which source substrates like rotting apples can be easily collected. We compared single host microbiomes with their corresponding apple source substrates, as well as nematode-free substrates, over a 2-year sampling period in the botanical garden in Kiel, Germany. We found that single worms have unique microbiomes, which overlap most strongly with nematodes from the same source apple. A comparison to previous, related work revealed that variation in microbiome composition of natural Caenorhabditis isolates is significantly influenced by the substrate type, from which worms were obtained (e.g., fruits or compost). Our current sampling further showed that microbiome assembly is mostly driven by dispersal limitation. Importantly, two independent analysis approaches consistently suggest that worm microbiomes significantly influence characteristics of the apple microbiomes, possibly indicating niche construction by nematodes. Moreover, combining apple microbiome and metabolome data, we identified individual microbes and specific compounds indicative of fruit ripening that are significantly associated with nematode presence. In conclusion, our study elucidates the complex relationship between host microbiomes and their directly connected substrate microbiomes. Our analyses underscore the significant influence of nematode microbiomes on shaping the apple microbiome and, consequently, the fruit's metabolic capacity, thereby enhancing our general understanding of host-microbiome interactions in their natural habitat.IMPORTANCEAlmost all complex organisms are host to a microbial community, the microbiome. This microbiome can influence diverse host functions, such as food processing, protection against parasites, or development. The relationship between host and microbiome critically depends on the assembly of the microbial community, which may be shaped by microbes in the directly linked environment, the source microbiome. This assembly process is often not well understood because of the unavailability of source substrates. Here, we used Caenorhabditis nematodes as a model system that facilitates a direct comparison of host and source microbiomes. Based on a 2-year sampling period, we identified (i) a clear link between assembly dynamics of host and source microbiomes, (ii) a significant influence of nematode microbiomes on apple microbiomes, and (iii) specific microbes and compounds that are associated with the presence of nematodes in the sampled substrates. Overall, our study enhances our understanding of microbiome assembly dynamics and resulting functions.

The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.

How a host’s microbiome changes over its lifespan can influence development and aging. As these temporal patterns have only been described in detail for a handful of hosts, an important next step is to compare microbiome succession more broadly and investigate why it varies. Here we characterize the temporal dynamics and stability of the bumble bee worker gut microbiome. Bumble bees have simple and host-specific gut microbiomes, and their microbial dynamics may influence health and pollination services. We used 16S rRNA gene sequencing, qPCR, and metagenomics to characterize gut microbiomes over the lifespan of Bombus impatiens workers. We also sequenced gut transcriptomes to examine host factors that may control the microbiome. At the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. But at the strain level, partitioning of bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome—including expression of key immunity genes—stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumble bees, maintenance of both microbiomes and immunity contribute to the inclusive fitness of workers, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession.

Host-associated microbiomes often promote host health, yet the key drivers of microbiome assembly and its consequences for host fitness remain unclear. We aimed to determine the relative roles of host identity versus the environment in driving host-microbiome assembly and the consequences of this variation in assembly for host fitness, which may help predict the resilience of host-associated microbiomes and host health amidst fluctuating environmental conditions. Here, we tracked microbiome assembly in association with initially axenic phytoplankton when incubated in seawater originating from four nearshore locations along a continental-scale environmental gradient of North America. Microbiome assembly was highly deterministic. Unexpectedly, host species identity was the overwhelming driver of microbiome community assembly despite continental-scale variation in the environment. Although secondary to host identity, the environment was a significant driver of microbiome assembly for each species evaluated, which, in turn, conferred cascading effects on host fitness as shown by thermal tolerance growth assays. We also found that host-specific microbiomes had host-specific fitness effects, particularly under thermally stressful conditions. Overall, our results advance our understanding of microbiome assembly by empirically demonstrating that although variation among host microbiomes imparted by the local environment has significant implications for host health, the host species is the overwhelming driver of microbiome assembly regardless of wide-scale variation in the environment.

In a plant-microbe symbiosis, the host plant plays a key role in promoting the association of beneficial microbes and maintaining microbiome homeostasis through microbe-associated molecular patterns (MAMPs). The associated microbes provide an additional layer of protection for plant immunity and help in nutrient acquisition. Despite identical MAMPs in pathogens and commensals, the plant distinguishes between them and promotes the enrichment of beneficial ones while defending against the pathogens. The rhizosphere is a narrow zone of soil surrounding living plant roots. Hence, various biotic and abiotic factors are involved in shaping the rhizosphere microbiome responsible for pathogen suppression. Efforts have been devoted to modifying the composition and structure of the rhizosphere microbiome. Nevertheless, systemic manipulation of the rhizosphere microbiome has been challenging, and predicting the resultant microbiome structure after an introduced change is difficult. This is due to the involvement of various factors that determine microbiome assembly and result in an increased complexity of microbial networks. Thus, a comprehensive analysis of critical factors that influence microbiome assembly in the rhizosphere will enable scientists to design intervention techniques to reshape the rhizosphere microbiome structure and functions systematically. In this review, we give highlights on fundamental concepts in soil suppressiveness and concisely explore studies on how plants monitor microbiome assembly and homeostasis. We then emphasize key factors that govern pathogen-suppressive microbiome assembly. We discuss how pathogen infection enhances plant immunity by employing a cry-for-help strategy and examine how domestication wipes out defensive genes in plants experiencing domestication syndrome. Additionally, we provide insights into how nutrient availability and pH determine pathogen suppression in the rhizosphere. We finally highlight up-to-date endeavors in rhizosphere microbiome manipulation to gain valuable insights into potential strategies by which microbiome structure could be reshaped to promote pathogen-suppressive soil development.

Microbial and abiotic factors of flooded soil that affect redox biodegradation of lindane

Plant microbiome assembly is a spatial and dynamic process driven by root exudates and influenced by soil type, plant developmental stage and genotype. Genotype-dependent microbiome assembly has been reported for different crop plant species. Despite the effect of plant genetics on microbiome assembly, the magnitude of host control over its root microbiome is relatively small or, for many plant species, still largely unknown. Here we cultivated modern and wild tomato genotypes for four successive cycles and showed that divergence in microbiome assembly between the two genotypes was significantly amplified over time. Also, we show that the composition of the rhizosphere microbiome of modern and wild plants became more dissimilar from the initial bulk soil and from each other. Co-occurrence analyses further identified amplicon sequence variants (ASVs) associated with early and late successions of the tomato rhizosphere microbiome. Among the members of the Late Successional Rhizosphere microbiome, we observed an enrichment of ASVs belonging to the genera Acidovorax, Massilia and Rhizobium in the wild tomato rhizosphere, whereas the modern tomato rhizosphere was enriched for an ASV belonging to the genus Pseudomonas. Collectively, our approach allowed us to study the dynamics of rhizosphere microbiome over successional cultivation as well as to categorize rhizobacterial taxa for their ability to form transient or long-term associations with their host plants.

Elucidating how plant-associated microbiome structure responds to nitrogen (N) and phosphorus (P) addition is crucial for predicting the impacts of anthropogenic disturbances on ecosystem functioning under global climate change scenarios. However, the differences in community assembly and bipartite network structure of phyllosphere and rhizosphere microbiomes under N and P addition are poorly understood. We investigated the microbiome (i.e. bacterial and fungal) communities in leaves and roots under N and P addition in a Chinese temperate meadow steppe. The results revealed that N and P addition significantly decreased the diversity and affected the community composition of bacteria and fungi in leaves and roots. The deterministic processes mainly governed the bacterial community assembly, whereas the stochastic processes primarily shaped the fungal community assembly in leaves and roots. The contribution of deterministic processes to bacterial community assembly was positively affected by N and P addition in leaves but negatively affected in roots. In contrast, the contribution of stochastic processes to fungal community assembly was negatively influenced by N and P addition in leaves but positively influenced in roots. The plant–bacterial and plant–fungal networks in both leaves and roots exhibited high specialization and modularity but low connectance and a lack of nestedness. Furthermore, N and P addition increased the complexity but decreased the stability of these networks. These findings demonstrate that N and P addition affects the community assembly and network structure of phyllosphere and rhizosphere microbiomes in the grassland ecosystem.

BackgroundMicrobiome assembly was identified as an important factor for plant growth and health, but this process is largely unknown, especially for the fruit microbiome. Therefore, we analyzed strawberry plants of two cultivars by focusing on microbiome tracking during the different growth stages and storage using amplicon sequencing, qPCR, and microscopic approaches.ResultsStrawberry plants carried a highly diverse microbiome, therein the bacterial families Sphingomonadaceae (25%), Pseudomonadaceae (17%), and Burkholderiaceae (11%); and the fungal family Mycosphaerella (45%) were most abundant. All compartments were colonized by high number of bacteria and fungi (107–1010 marker gene copies per g fresh weight), and were characterized by high microbial diversity (6049 and 1501 ASVs); both were higher for the belowground samples than in the phyllosphere. Compartment type was the main driver of microbial diversity, structure, and abundance (bacterial: 45%; fungal: 61%) when compared to the cultivar (1.6%; 2.2%). Microbiome assembly was strongly divided for belowground habitats and the phyllosphere; only a low proportion of the microbiome was transferred from soil via the rhizosphere to the phyllosphere. During fruit development, we observed the highest rates of microbial transfer from leaves and flowers to ripe fruits, where most of the bacteria occured inside the pulp. In postharvest fruits, microbial diversity decreased while the overall abundance increased. Developing postharvest decay caused by Botrytis cinerea decreased the diversity as well, and induced a reduction of potentially beneficial taxa.ConclusionOur findings provide insights into microbiome assembly in strawberry plants and highlight the importance of microbe transfer during fruit development and storage with potential implications for food health and safety.

BackgroundThe plant microbiome can support plant health and fitness in the face of biotic and abiotic stress. Research has mostly focused on plant growth in natural and agricultural soils. However, as urban areas continue to expand and soils change in the Anthropocene, microbiome assembly during development of plants grown in urban area soil remains largely elusive. Here, we examined the effect of developmental stages on the phyllosphere and rhizosphere microbiomes of rice grown in soil from an urban area during the vegetative growth stages.ResultsWe found that the microbial alpha and beta diversity, networks, and functions of the phyllosphere and rhizosphere microbiomes significantly differed among rice seedling, tillering, and elongation stages. Notably, we observed that bacteria assigned to potential animal parasites or symbionts not only exhibited significantly higher relative abundances in the phyllosphere compared to the rhizosphere but are also influenced by the developmental stages. Plants grown in the urban area soil had a higher relative abundance of Bacteroidales and enriched bacteria assigned to potential animal parasites or symbionts in the phyllosphere in contrast to plants grown in field. Some of these bacteria were shown to significantly influence the assembly of the phyllosphere microbiome and to prevalently engage in negative interactions with other microbes.ConclusionOur study provides new insights into developmental stage-resolved microbiome assembly of plants grown in urban areas. The insights could help in the development of strategies for promoting ‘One Health’ by highlighting the role of plants as alternative host for bacterial groups that are prevalently associated with animals.

Humans consider themselves discrete autonomous organisms, but recent research is rapidly strengthening the appreciation that associated microorganisms make essential contributions to human health and well being. Each person is inhabited and also surrounded by his/her own signature microbial cloud. A low diversity of microorganisms is associated with a plethora of diseases, including allergy, diabetes, obesity, arthritis, inflammatory bowel diseases, and even neuropsychiatric disorders. Thus, an interaction of microorganisms with the host immune system is required for a healthy body. Exposure to microorganisms from the moment we are born and appropriate microbiome assembly during childhood are essential for establishing an active immune system necessary to prevent disease later in life. Exposure to microorganisms educates the immune system, induces adaptive immunity, and initiates memory B and T cells that are essential to combat various pathogens. The correct microbial-based education of immune cells may be critical in preventing the development of autoimmune diseases and cancer. This review provides a broad overview of the importance of the host microbiome and accumulating knowledge of how it regulates and maintains a healthy human system. Cancer Res; 77(8); 1783-812. ©2017 AACR.

Crop-dependent root-microbe-soil interactions induce contrasting natural attenuation of organochlorine lindane in soils

Protists: Puppet Masters of the Rhizosphere Microbiome

Temporal metabolite responsiveness of microbiota in the tea plant phyllosphere promotes continuous suppression of fungal pathogens

The research presented in this thesis aims at improving our understanding of rhizosphere microbiome assembly under drought through three comparative studies between different plants, at three different evolutionary scales, addressing both common and different research questions. Overall, I aim to shed light on rhizosphere microbiome assembly under drought by focusing on (i) commonalities and differences between different plants, (ii) evolutionary patterns and (iii) plant mechanisms shaping this microbiome.In chapter 1, the general introduction, I present the current state of knowledge on the rhizosphere microbiome and how it is shaped by plants, in particular through root exudation. This is also placed in an evolutionary context. I then elaborate how plants and the rhizosphere microbiome respond to drought stress, and how their interaction affects plant fitness and drought resilience.In chapter 2, we study the microbiome associated with the rhizoids, named rhizoid-sphere, of three bryophyte plant species. We compare these microbiomes and their changes under drought between these three species and with two angiosperm species. This reveals some consistent compositional changes in the rhizosphere microbiome under drought. We also show that certain bacterial taxa known for their plant growth promoting properties show strong differences in abundance between bryophyte species, suggesting that the interaction with these bacterial taxa may have evolved at an early stage of land plant evolution.In chapter 3, we compare the rhizosphere microbiome of 24 different plant species under drought and well-watered conditions. We show that these microbiomes show very similar compositional shifts under drought, but also some differences, which we correlate with the host plant species’ drought resilience. We also show that host species specificity patterns of rhizosphere microbes can be linked to the host plants’ phylogeny, but this pattern is weakened under drought. Lastly, we correlate rhizosphere microbiome data with untargeted liquid chromatography – mass spectrometry (LC-MS) of root metabolites to generate hypotheses regarding specific root metabolites that may play a role in the recruitment of specific microbial taxa in the rhizosphere.In chapter 4, we zoom into intra-species variation in the rhizosphere microbiome of tomato. We analyze the rhizosphere microbiomes associated with 139 different tomato genotypes, under drought and well-watered conditions. We show differences in these tomato genotypes’ rhizosphere microbiome composition and link them to host genotype dissimilarity. Like in chapter 3, we show that this link is weakened under drought. We further identify which bacterial taxa show a high heritability, i.e. of which the relative abundance is strongly influenced by the host genotype. Finally, we perform genome-wide association studies (GWAS) to identify plant genetic loci associated with plant biomass and drought resilience, and with the relative abundance of specific bacteria in the rhizosphere.In chapter 5, the general discussion, I draw some parallels between the three experimental chapters and put the research presented in this thesis in the context of the latest scientific literature. I further discuss how fundamental research on the rhizosphere microbiome can feed into applied research and give an outlook on its potential impact on agriculture.