Summary
Plant microbiomes are essential to host health and productivity but the ecological processes that govern crop microbiome assembly are not fully known.
Here we examined bacterial communities ...across 684 samples from soils (rhizosphere and bulk soil) and multiple compartment niches (rhizoplane, root endosphere, phylloplane, and leaf endosphere) in maize (Zea mays)‐wheat (Triticum aestivum)/barley (Hordeum vulgare) rotation system under different fertilization practices at two contrasting sites.
Our results demonstrate that microbiome assembly along the soil‐plant continuum is shaped predominantly by compartment niche and host species rather than by site or fertilization practice. From soils to epiphytes to endophytes, host selection pressure sequentially increased and bacterial diversity and network complexity consequently reduced, with the strongest host effect in leaf endosphere. Source tracking indicates that crop microbiome is mainly derived from soils and gradually enriched and filtered at different plant compartment niches. Moreover, crop microbiomes were dominated by a few dominant taxa (c. 0.5% of bacterial phylotypes), with bacilli identified as the important biomarker taxa for wheat and barley and Methylobacteriaceae for maize.
Our work provides comprehensive empirical evidence on host selection, potential sources and enrichment processes for crop microbiome assembly, and has important implications for future crop management and manipulation of crop microbiome for sustainable agriculture.
Summary
Plants harbour highly diverse mycobiomes which sustain essential functions for host health and productivity. However, ecological processes that govern the plant–mycobiome assembly, ...interactions and their impact on ecosystem functions remain poorly known. Here we characterized the ecological role and community assembly of both abundant and rare fungal taxa along the soil–plant continuums (rhizosphere, phyllosphere and endosphere) in the maize–wheat/barley rotation system under different fertilization practices at two contrasting sites. Our results indicate that mycobiome assembly is shaped predominantly by compartment niche and host species rather than by environmental factors. Moreover, crop‐associated fungal communities are dominated by few abundant taxa mainly belonging to Sordariomycetes and Dothideomycetes, while the majority of diversity within mycobiomes are represented by rare taxa. For plant compartments, the abundant sub‐community is mainly determined by stochastic processes. In contrast, the rare sub‐community is more sensitive to host selection and mainly governed by deterministic processes. Furthermore, our results demonstrate that rare taxa play an important role in fungal co‐occurrence network and ecosystem functioning like crop yield and soil enzyme activities. These results significantly advance our understanding of crop mycobiome assembly and highlight the key role of rare taxa in sustaining the stability of crop mycobiomes and ecosystem functions.
Summary
Plants form complex interaction networks with diverse microbiomes in the environment, and the intricate interplay between plants and their associated microbiomes can greatly influence ...ecosystem processes and functions. The phyllosphere, the aerial part of the plant, provides a unique habitat for diverse microbes, and in return the phyllosphere microbiome greatly affects plant performance. As an open system, the phyllosphere is subjected to environmental perturbations, including global change, which will impact the crosstalk between plants and their microbiomes. In this review, we aim to provide a synthesis of current knowledge of the complex interactions between plants and the phyllosphere microbiome under global changes and to identify future priority areas of research on this topic.
Summary
Viruses can affect microbial dynamics, metabolism and biogeochemical cycles in aquatic ecosystems. However, viral diversity and functions in agricultural soils are poorly known, especially in ...the rhizosphere. We used virome analysis of eight rhizosphere and bulk soils to study viral diversity and potential biogeochemical impacts in an agro‐ecosystem. The order Caudovirales was the predominant viral type in agricultural soils, with Siphoviridae being the most abundant family. Phylogenetic analysis of the terminase large subunit of Caudovirales identified high viral diversity and three novel groups. Viral community composition differed significantly between bulk and rhizosphere soils. Soil pH was the main environmental driver of the viral community structure. Remarkably, abundant auxiliary carbohydrate‐active enzyme (CAZyme) genes were detected in viromes, including glycoside hydrolases, carbohydrate esterases and carbohydrate‐binding modules. These results demonstrate that virus‐encoded putative auxiliary metabolic genes or metabolic genes that may change bacterial metabolism and indirectly contribute to biogeochemical cycling, especially carbon cycling, in agricultural soil.
Agricultural food production is at the base of food and fodder, with fertilization having fundamentally and continuously increased crop yield over the last decades. The performance of crops is ...intimately tied to their microbiome as they together form holobionts. The importance of the microbiome for plant performance is, however, notoriously ignored in agricultural systems as fertilization disconnects the dependency of plants for often plant-beneficial microbial processes. Moreover, we lack a holistic understanding of how fertilization regimes affect the soil microbiome. Here, we examined the effect of a 2-year fertilization regime (no nitrogen fertilization control, nitrogen fertilization, and nitrogen fertilization plus straw amendment) on entire soil microbiomes (bacteria, fungi, and protist) in three common agricultural soil types cropped with maize in two seasons.
We found that the application of nitrogen fertilizers more strongly affected protist than bacterial and fungal communities. Nitrogen fertilization indirectly reduced protist diversity through changing abiotic properties and bacterial and fungal communities which differed between soil types and sampling seasons. Nitrogen fertilizer plus straw amendment had greater effects on soil physicochemical properties and microbiome diversity than nitrogen addition alone. Moreover, nitrogen fertilization, even more together with straw, increased soil microbiome network complexity, suggesting that the application of nitrogen fertilizers tightened soil microbiomes interactions.
Together, our results suggest that protists are the most susceptible microbiome component to the application of nitrogen fertilizers. As protist communities also exhibit the strongest seasonal dynamics, they serve as the most sensitive bioindicators of soil changes. Changes in protist communities might have long-term effects if some of the key protist hubs that govern microbiome complexities as top microbiome predators are altered. This study serves as the stepping stone to promote protists as promising agents in targeted microbiome engineering to help in reducing the dependency on exogenous unsustainably high fertilization and pesticide applications.
Increasing evidence demonstrated the involvement of ammonia-oxidizing archaea (AOA) in the global nitrogen cycle, but the relative contributions of AOA and ammonia-oxidizing bacteria (AOB) to ammonia ...oxidation are still in debate. Previous studies suggest that AOA would be more adapted to ammonia-limited oligotrophic conditions, which seems to be favored by protonation of ammonia, turning into ammonium in low-pH environments. Here, we investigated the autotrophic nitrification activity of AOA and AOB in five strongly acidic soils (pH<4.50) during microcosm incubation for 30 days. Significantly positive correlations between nitrate concentration and amoA gene abundance of AOA, but not of AOB, were observed during the active nitrification. (13)CO(2)-DNA-stable isotope probing results showed significant assimilation of (13)C-labeled carbon source into the amoA gene of AOA, but not of AOB, in one of the selected soil samples. High levels of thaumarchaeal amoA gene abundance were observed during the active nitrification, coupled with increasing intensity of two denaturing gradient gel electrophoresis bands for specific thaumarchaeal community. Addition of the nitrification inhibitor dicyandiamide (DCD) completely inhibited the nitrification activity and CO(2) fixation by AOA, accompanied by decreasing thaumarchaeal amoA gene abundance. Bacterial amoA gene abundance decreased in all microcosms irrespective of DCD addition, and mostly showed no correlation with nitrate concentrations. Phylogenetic analysis of thaumarchaeal amoA gene and 16S rRNA gene revealed active (13)CO(2)-labeled AOA belonged to groups 1.1a-associated and 1.1b. Taken together, these results provided strong evidence that AOA have a more important role than AOB in autotrophic ammonia oxidation in strongly acidic soils.
Abstract
Background
Plants live with diverse microbial communities which profoundly affect multiple facets of host performance, but if and how host development impacts the assembly, functions and ...microbial interactions of crop microbiomes are poorly understood. Here we examined both bacterial and fungal communities across soils, epiphytic and endophytic niches of leaf and root, and plastic leaf of fake plant (representing environment-originating microbes) at three developmental stages of maize at two contrasting sites, and further explored the potential function of phylloplane microbiomes based on metagenomics.
Results
Our results suggested that plant developmental stage had a much stronger influence on the microbial diversity, composition and interkingdom networks in plant compartments than in soils, with the strongest effect in the phylloplane. Phylloplane microbiomes were co-shaped by both plant growth and seasonal environmental factors, with the air (represented by fake plants) as its important source. Further, we found that bacterial communities in plant compartments were more strongly driven by deterministic processes at the early stage but a similar pattern was for fungal communities at the late stage. Moreover, bacterial taxa played a more important role in microbial interkingdom network and crop yield prediction at the early stage, while fungal taxa did so at the late stage. Metagenomic analyses further indicated that phylloplane microbiomes possessed higher functional diversity at the early stage than the late stage, with functional genes related to nutrient provision enriched at the early stage and N assimilation and C degradation enriched at the late stage. Coincidently, more abundant beneficial bacterial taxa like Actinobacteria,
Burkholderiaceae
and
Rhizobiaceae
in plant microbiomes were observed at the early stage, but more saprophytic fungi at the late stage.
Conclusions
Our results suggest that host developmental stage profoundly influences plant microbiome assembly and functions, and the bacterial and fungal microbiomes take a differentiated ecological role at different stages of plant development. This study provides empirical evidence for host exerting strong effect on plant microbiomes by deterministic selection during plant growth and development. These findings have implications for the development of future tools to manipulate microbiome for sustainable increase in primary productivity.
Summary
Terrestrial–marine boundaries are significant sites of biogeochemical activity with delineated gradients from land to sea. While niche differentiation of ammonia‐oxidizing archaea (AOA) and ...bacteria (AOB) driven by pH and nitrogen is well known, the patterns and environmental drivers of AOA and AOB community structure and activity across soil‐sediment boundaries have not yet been determined. In this study, nitrification potential rate, community composition and transcriptional activity of AOA and AOB in soil, soil/sediment interface and sediments of two coastal Bays were characterized using a combination of field investigations and microcosm incubations. At DNA level, amoA gene abundances of AOA were significantly greater than AOB in soil, while in sediments AOB were significantly more abundant than AOA, but at the soil/sediment interface there were equal numbers of AOA and AOB amoA genes. Microcosm incubations provided further evidence, through qPCR and DGGE‐sequencing analysis of amoA transcripts, that AOA were active in soil, AOB in sediment and both AOA and AOB were active at the soil/sediment interface. The AOA and AOB community composition shifted across the coastal soil‐interface‐sediment gradient with salinity and pH identified as major environmental drivers.
The abundance and composition of soil ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) communities under different long-term (17 years) fertilization practices were investigated ...using real-time polymerase chain reaction and denaturing gradient gel electrophoresis (DGGE). A sandy loam with pH (H₂O) ranging from 8.3 to 8.7 was sampled in years 2006 and 2007, including seven fertilization treatments of control without fertilizers (CK), those with combinations of fertilizer nitrogen (N), phosphorus (P) and potassium (K): NP, NK, PK and NPK, half chemical fertilizers NPK plus half organic manure (1/2OMN) and organic manure (OM). The highest bacterial amoA gene copy numbers were found in those treatments receiving N fertilizer. The archaeal amoA gene copy numbers ranging from 1.54 x 10⁷ to 4.25 x 10⁷ per gram of dry soil were significantly higher than those of bacterial amoA genes, ranging from 1.24 x 10⁵ to 2.79 x 10⁶ per gram of dry soil, which indicated a potential role of AOA in nitrification. Ammonia-oxidizing bacteria abundance had significant correlations with soil pH and potential nitrification rates. Denaturing gradient gel electrophoresis patterns revealed that the fertilization resulted in an obvious change of the AOB community, while no significant change of the AOA community was observed among different treatments. Phylogenetic analysis showed a dominance of Nitrosospira-like sequences, while three bands were affiliated with the Nitrosomonas genus. All AOA sequences fell within cluster S (soil origin) and cluster M (marine and sediment origin). These results suggest that long-term fertilization had a significant impact on AOB abundance and composition, while minimal on AOA in the alkaline soil.
The soil microbiome determines crop production and drives nutrient cycling, functions that are altered by fertilization. Yet, we have only begun to understand the effects of fertilization on ...taxonomic changes on soil microorganisms, while impacts on functional groups across the microbiome and therefore potential soil functioning have never been assessed. Here, using a range of methods including high-throughput sequencing, we identified 77 functional parameters of the main microbiome groups including bacteria, fungi, and protists in three common agricultural soil types in China (black, fluvo-aquic, and red soil), which were fertilized in the same way over two years. We show that fertilization most strongly and generally throughout soil types reduced the relative abundance of the main microbial predators, phagotrophic protists, by 31%. Ten functional groups within the microbiome showed soil type-specific responses to fertilization. For example, ammonia-oxidizing bacteria, and predatory/exoparasitic bacteria were reduced by fertilization in the acidic black and the red soils, while, no other microbial functional group than phagotrophic protists was suppressed by fertilization in the alkaline fluvo-aquic soil. The significant reductions in microbial functional groups especially in acidic soils could be explained by nitrogen enrichment, increased soil acidification and potential biotic links between the functional groups within the microbiome. Together, we show that the fertilization-induced abiotic changes alter microbial functions that depend on the soil and environmental conditions. Particularly the most profound changes on the group of microbial predators might subsequently affect other soil functions performed by bacteria and fungi.
•Microbiome functioning was affected by fertilization in a soil-specific manner.•Fertilization reduced AOB and predatory/exoparasitic bacteria in acidic soils.•Only phagotrophic protists were suppressed by fertilization across all soil types.•Fertilizer-induced changes on protists likely alter entire microbiome functioning.
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