Unveiling the overlooked microbial niches thriving on building exteriors.

Rapid urbanization in the Asia-Pacific region is expected to place two-thirds of its population in concrete-dominated urban landscapes by 2050. While diverse architectural facades define the unique appearance of these urban systems. There remains a significant gap in our understanding of the composition, assembly, and ecological potential of microbial communities on building exteriors. Here, we examined bacterial and protistan communities on building surfaces along an urbanization gradient (urban, suburban and rural regions), investigating their spatial patterns and the driving factors behind their presence. A total of 55 bacterial and protist phyla were identified. The bacterial community was predominantly composed of Proteobacteria (33.7% to 67.5%). The protistan community exhibited a prevalence of Opisthokonta and Archaeplastida (17.5% to 82.1% and 1.8% to 61.2%, respectively). The composition and functionality of bacterial communities exhibited spatial patterns correlated with urbanization. In urban buildings, factors such as facade type, light exposure, and building height had comparatively less impact on bacterial composition compared to suburban and rural areas. The highest bacterial diversity and lowest Weighted Average Community Identity (WACI) were observed on suburban buildings, followed by rural buildings. In contrast, protists did not show spatial distribution characteristics related to facade type, light exposure, building height and urbanization level. The distinct spatial patterns of protists were primarily shaped by community diffusion and the bottom-up regulation exerted by bacterial communities. Together, our findings suggest that building exteriors serve as attachment points for local microbial metacommunities, offering unique habitats where bacteria and protists exhibit independent adaptive strategies closely tied to the overall ecological potential of the community.

Assembly and succession of the phyllosphere microbiome and nutrient-cycling genes during plant community development in a glacier foreland.

The phyllosphere, particularly the leaf surface of plants, harbors a diverse range of microbiomes that play a vital role in the functioning of terrestrial ecosystems. However, our understanding of microbial successions and their impact on functional genes during plant community development is limited. In this study, considering core and satellite microbial taxa, we characterized the phyllosphere microbiome and functional genes in various microhabitats (i.e., leaf litter, moss and plant leaves) across the succession of a plant community in a low-altitude glacier foreland. Our findings indicate that phyllosphere microbiomes and associated ecosystem stability increase during the succession of the plant community. The abundance of core taxa increased with plant community succession and was primarily governed by deterministic processes. In contrast, satellite taxa abundance decreased during plant community succession and was mainly governed by stochastic processes. The abundance of microbial functional genes (such as C, N, and P hydrolysis and fixation) in plant leaves generally increased during the plant community succession. However, in leaf litter and moss leaves, only a subset of functional genes (e.g., C fixation and degradation, and P mineralization) showed a tendency to increase with plant community succession. Ultimately, the community of both core and satellite taxa collaboratively influenced the characteristics of phyllosphere nutrient-cycling genes, leading to the diverse profiles and fluctuating abundance of various functional genes during plant community succession. These findings offer valuable insights into the phyllosphere microbiome and plant-microbe interactions during plant community development, advancing our understanding of the succession and functional significance of the phyllosphere microbial community.

National-scale investigation reveals the dominant role of phyllosphere fungal pathogens in sorghum yield loss.

Fungal plant pathogens threaten crop production and sustainable agricultural development. However, the environmental factors driving their diversity and nationwide biogeographic model remain elusive, impacting our capacity to predict their changes under future climate scenarios. Here, we analyzed potential fungal plant pathogens from 563 samples collected from 57 agricultural fields across China. Over 28.0% of fungal taxa in the phyllosphere were identified as potential plant pathogens, compared to 22.3% in the rhizosphere. Dominant fungal plant pathogen groups were Cladosporium (in the phyllosphere) and Fusarium (in the rhizosphere), with higher diversity observed in the phyllosphere than in rhizosphere soil. Deterministic processes played an important role in shaping the potential fungal plant pathogen community assembly in both habitats. Mean annual precipitation and temperature were the most important factor influencing phyllosphere fungal plant pathogen richness. Significantly negative relationships were found between fungal pathogen diversity and sorghum yield. Notably, compared to the rhizosphere, the phyllosphere fungal plant pathogen diversity played a more crucial role in sorghum yield. Together, our work provides novel insights into the factors governing the spatial patterns of fungal plant pathogens in the crop microbiome, and highlights the potential significance of aboveground phyllosphere fungal plant pathogens in crop productivity.

Aboveground plants determine the exchange of pathogens within air-phyllosphere-soil continuum in urban greenspaces.

The microbiome in the air-phyllosphere-soil continuum of urban greenspaces plays a crucial role in re-connecting urban populations with biodiverse environmental microbiomes. However, little is known about whether plant type affects the airborne microbiomes, as well as the extent to which soil and phyllosphere microbiomes contribute to airborne microbiomes. Here we collected soil, phyllosphere and airborne microbes with different plant types (broadleaf tree, conifer tree, and grass) in urban parks. Despite the significant impacts of plant type on soil and phyllosphere microbiomes, plant type had no obvious effects on the diversity of airborne microbes but shaped airborne bacterial composition in urban greenspaces. Soil and phyllosphere microbiomes had a higher contribution to airborne bacteria in broadleaf trees (37.56%) compared to conifer trees (9.51%) and grasses (14.29%). Grass areas in urban greenspaces exhibited a greater proportion of potential pathogens compared to the tree areas. The abundance of bacterial pathogens in phyllosphere was significantly higher in grasses compared to broadleaf and conifer trees. Together, our study provides novel insights into the microbiome patterns in air-phyllosphere-soil continuum, highlighting the potential significance of reducing the proportion of extensively human-intervened grass areas in future urban environment designs to enhance the provision of ecosystem services in urban greenspaces.

Protistan predation selects for antibiotic resistance in soil bacterial communities.

Understanding how antibiotic resistance emerges and evolves in natural habitats is critical for predicting and mitigating antibiotic resistance in the context of global change. Bacteria have evolved antibiotic production as a strategy to fight competitors, predators and other stressors, but how predation pressure of their most important consumers (i.e., protists) affects soil antibiotic resistance genes (ARGs) profiles is still poorly understood. To address this gap, we investigated responses of soil resistome to varying levels of protistan predation by inoculating low, medium and high concentrations of indigenous soil protist suspensions in soil microcosms. We found that an increase in protistan predation pressure was strongly associated with higher abundance and diversity of soil ARGs. High protist concentrations significantly enhanced the abundances of ARGs encoding multidrug (oprJ and ttgB genes) and tetracycline (tetV) efflux pump by 608%, 724% and 3052%, respectively. Additionally, we observed an increase in the abundance of numerous bacterial genera under high protistan pressure. Our findings provide empirical evidence that protistan predation significantly promotes antibiotic resistance in soil bacterial communities and advances our understanding of the biological driving forces behind the evolution and development of environmental antibiotic resistance.

Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil-water continuum.

Rice paddy soil is a hotspot of antibiotic resistance genes (ARGs) due to the application of organic fertilizers. However, the temporal dynamics of ARGs in rice paddy soil and its flooded water during the growing season remain underexplored. In this study, a microcosm experiment was conducted to explore the ARG profiles in a long term (130 days) flooded two-phase manure-amended soil-water system. By using high-throughput quantitative PCR array, a total of 23-98 and 34-85 ARGs were detected in the soil and overlying water, respectively. Regression analysis exhibited significant negative correlations between ARG profile similarities and flooding duration, indicating that flooding significantly altered the resistome (P < 0.001). This finding was validated by the increased ARG abundance in the soil and the overlying water, for example, after 130 days flooding, the abundance of ARGs in CK soil was increased from 0.03 to 1.20 copies per 16S rRNA. The PCoA analysis further suggested pig manure application resulted in distinct ARG profiles in the soil-water continuum compared with those of the non-amended control (Adonis, P < 0.05). The Venn diagram showed that all ARGs detected in the pig manure were present in the treated soil. Twelve ARGs (e.g., sul1) were shared among the pig manure, manure-amended soil, and overlying water, indicating that certain manure- or soil-borne ARGs were readily dispersed from the soil to the overlying water. Moreover, the enhanced relationships between the ARGs and mobile genetic elements in pig manure applied soil-water continuum indicate that the application of organic matter could accelerate the emergence and dissemination of ARGs. These findings suggested that flooding represents a crucial pathway for dispersal of ARGs from the soil to the overlying water. Identification of highly mobile ARGs in the soil-water continuum is essential for assessing their potential risk to human health and promoting the development of sustainable agricultural practices to mitigate their spread.

Brand-Specific Toxicity of Tire Tread Particles Helps Identify the Determinants of Toxicity.

The widespread occurrence of tire tread particles (TPs) has aroused increasing concerns over their impacts. However, how they affect the soil fauna remains poorly understood. Here, based on systematically assessing the toxicity of TPs on soil model speciesEnchytraeus crypticusat environmentally relevant concentrations through both soil and food exposure routes, we reported that TPs affected gut microbiota, intestinal histopathology, and metabolites of the worms both through particulate- and leachate-induced effects, while TP leachates exerted stronger effects. The dominant role of TP leachates in TP toxicity was further explained by the findings that worms did not ingest TPs with a particle size of over 150 µm and actively avoided consuming TP particles. Moreover, by comparing the effects of different brands of TPs as well as new and aged TPs, we demonstrated that it was mainly TP leachates that resulted in the ubiquity of the disturbance in the worm's gut microbiota among different brands of TPs. Notably, the large variations in leachate compositions among different brands of TPs provided us a unique opportunity to identify the determinants of TP toxicity. These results provide novel insights into the toxicity of TPs to soil fauna and a reference for toxicity reduction of tires.

Trophic interrelationships of bacteria are important for shaping soil protist communities.

Protists occupy multiple trophic positions in soil food webs and significantly contribute to organic matter decomposition and biogeochemical cycling. Protists can ingest bacteria and fungi as main food sources while being subjected to predation of invertebrates, but our understanding of how bottom-up and top-down regulations structure protists in natural soil habitats is limited. Here, we disentangle the effects of trophic regulations to the diversity and structure of soil protists in natural settings across northern and eastern Australia. Bacterial and invertebrate diversity were identified as important drivers of the diversity of functional groups of protists. Moreover, the compositions of protistan taxonomic and functional groups were better predicted by bacteria and fungi, than by soil invertebrates. There were strong trophic interconnections between protists and bacteria in multiple organismic network analysis. Altogether, the study provided new evidence that, bottom-up control of bacteria played an important role in shaping the soil protist community structure, which can be derived from feeding preferences of protists on microbial prey, and their intimate relationships in soil functioning or environmental adaptation. Our findings advance our knowledge about the impacts of different trophic groups on key soil organismic communities, with implications for ecosystem functions and services.

Temporal dynamics of soil bacterial network regulate soil resistomes.

Soil bacteria are diverse and form complicated ecological networks through various microbial interactions, which play important roles in soil multi-functionality. However, the seasonal effects on the bacterial network, especially the relationship between bacterial network topological features and soil resistomes remains underexplored, which impedes our ability to unveil the mechanisms of the temporal-dynamics of antibiotic resistance genes (ARGs). Here, a field investigation was conducted across four seasons at the watershed scale. We observed significant seasonal variation in bacterial networks, with lower complexity and stability in autumn, and a wider bacterial community niche in summer. Similar to bacterial communities, the co-occurrence networks among ARGs also shift with seasonal change, particularly with respect to the topological features of the node degree, which on average was higher in summer than in the other seasons. Furthermore, the nodes with higher betweenness, stress, degree, and closeness centrality in the bacterial network showed strong relationships with the 10 major classes of ARGs. These findings highlighted the changes in the topological properties of bacterial networks that could further alter antibiotic resistance in soil. Together, our results reveal the temporal dynamics of bacterial ecological networks at the watershed scale, and provide new insights into antibiotic resistance management under environmental changes.

The global distribution and environmental drivers of the soil antibiotic resistome.

BACKGROUND: Little is known about the global distribution and environmental drivers of key microbial functional traits such as antibiotic resistance genes (ARGs). Soils are one of Earth's largest reservoirs of ARGs, which are integral for soil microbial competition, and have potential implications for plant and human health. Yet, their diversity and global patterns remain poorly described. Here, we analyzed 285 ARGs in soils from 1012 sites across all continents and created the first global atlas with the distributions of topsoil ARGs. RESULTS: We show that ARGs peaked in high latitude cold and boreal forests. Climatic seasonality and mobile genetic elements, associated with the transmission of antibiotic resistance, were also key drivers of their global distribution. Dominant ARGs were mainly related to multidrug resistance genes and efflux pump machineries. We further pinpointed the global hotspots of the diversity and proportions of soil ARGs. CONCLUSIONS: Together, our work provides the foundation for a better understanding of the ecology and global distribution of the environmental soil antibiotic resistome. Video Abstract.

Aridity differentially alters the stability of soil bacterial and fungal networks in coastal and inland areas of Australia.

Despite the importance of soil bacterial and fungal communities for ecosystem services and human welfare, how their ecological networks respond to climatic aridity have yet been evaluated. Here, we collected soil samples from 47 sites across 2500 km in coastal and inland areas of eastern Australia with contrasting status of aridity. We found that the diversity of both bacteria and fungi significantly differed between inland and coastal soils. Despite the significant differences in soil nutrient availability and stoichiometry between the inland and coastal regions, aridity was the most important predictor of bacterial and fungal community compositions. Aridity has altered the potential microbial migration rates and further impacted the microbial assembly processes by increasing the importance of stochasticity in bacterial and fungal communities. More importantly, ecological network analysis indicated that aridity enhanced the complexity and stability of the bacterial network but reduced that of the fungal network, possibly due to the contrasting impacts of aridity on the community-level habitat niche breadth and overlaps. Our work paves the way towards a more comprehensive understanding of how climate changes will alter soil microbial communities, which is integral to predicting their long-term consequences for ecosystem sustainability and resilience to future disturbances.

Soil mesofauna alter the balance between stochastic and deterministic processes in the plastisphere during microbial succession.

Plastic debris, as a novel substrate, provides an avenue for enriching microbial growth. Although the structure of the aquatic plastisphere microbial community is well-characterised, linkages between microbial community assembly and species co-existence in the soil plastisphere vary and remain poorly understood, particularly when soil fauna is involved. This study investigated the soil plastisphere community, including bacteria, fungi, and protists, focusing on microbial succession and community assembly processes impacted by soil mesofauna. Certain soil plastisphere microbial taxa thrived at particular time points (e.g. Actinobacteria at 60 d), indicating the irreplaceable role of microplastic selection for time-sensitive taxa. Additionally, the biodiversity of keystone ecological clusters in the soil plastisphere was significantly associated with incubation time. Furthermore, the slopes of bacterial and fungal time-decay curves in soil plastisphere were steeper when treated with soil mesofauna than without soil mesofauna, whereas protist time-decay curves (total and abundant taxa) exhibited the opposite trend. Soil mesofauna increased the relative importance of determinacy in the soil plastisphere bacterial assembly process, while enhancing the stochasticity of fungal and protistan community assemblages. The study demonstrates the complex assembly patterns of soil plastisphere microbial communities, emphasising the importance of interactions between the plastisphere and local soil fauna from an ecological perspective.

Microbial Multitrophic Communities Drive the Variation of Antibiotic Resistome in the Gut of Soil Woodlice (Crustacea: Isopoda).

Multitrophic communities inhabit in soil faunal gut, including bacteria, fungi, and protists, which have been considered a hidden reservoir for antibiotic resistance genes (ARGs). However, there is a dearth of research focusing on the relationships between ARGs and multitrophic communities in the gut of soil faunas. Here, we studied the contribution of multitrophic communities to variations of ARGs in the soil woodlouse gut. The results revealed diverse and abundant ARGs in the woodlouse gut. Network analysis further exhibited strong connections between key ecological module members and ARGs, suggesting that multitrophic communities in the keystone ecological cluster may play a pivotal role in the variation of ARGs in the woodlouse gut. Moreover, long-term application of sewage sludge significantly altered the woodlice gut resistome and interkingdom communities. The variation portioning analysis indicated that the fungal community has a greater contribution to variations of ARGs than bacterial and protistan communities in the woodlice gut after long-term application of sewage sludge. Together, our results showed that changes in gut microbiota associated with agricultural practices (e.g., sewage sludge application) can largely alter the gut interkingdom network in ecologically relevant soil animals, with implications for antibiotic resistance, which advances our understanding of the microecological drivers of ARGs in terrestrial ecosystem.

Semi-solid state promotes the methane production during anaerobic co-digestion of chicken manure with corn straw comparison to wet and high-solid state.

Total solid content (TS) is an important factor for biogas production during anaerobic digestion. In this study, we explored the influence of different TS (5% wet, 15% semi-solid and 25% solid state) on the relative cumulative methane production (RCMP) during anaerobic co-digestion of chicken manure with corn straw. Results showed that total ammonium nitrogen and free ammonia nitrogen concentration increased with the increase of TS. Ammonium nitrogen in treatments at 15% TS was 2.25-2.76 times as high as that at 5% TS, which was below 3 times. The highest chemical oxygen demand removal and RCMP were obtained in the treatment of 15% TS with a ratio of 2:1 chicken manure: corn straw (based on TS). The RCMP in the treatments of 15% TS were 3.63-4.59 times higher than that of 5% TS based on the volume of substrates. The abundance of Caldicoprobacter improving the degradation of corn straw was significantly positively correlated with the RCMP, and the average abundance of Caldicoprobacter at 15% TS was 8.33 and 7.02 times higher than that at 5% and 25% TS, respectively. Structural equation models analysis suggested that TS significantly impacted the RCMP by indirectly impacting free ammonia nitrogen and microbial abundance. These findings indicated semi-solid state (15% TS) decreased ammonia nitrogen releasing and improved the abundance of Caldicoprobacter, and increased RCMP during anaerobic co-digestion of chicken manure with corn straw.

Cross-biome antibiotic resistance decays after millions of years of soil development.

Soils harbor the most diverse naturally evolved antibiotic resistance genes (ARGs) on Earth, with implications for human health and ecosystem functioning. How ARGs evolve as soils develop over centuries, to millennia (i.e., pedogenesis), remains poorly understood, which introduces uncertainty in predictions of the dynamics of ARGs under changing environmental conditions. Here we investigated changes in the soil resistome by analyzing 16 globally distributed soil chronosequences, from centuries to millennia, spanning a wide range of ecosystem types and substrate age ranges. We show that ARG abundance and diversity decline only after millions of years of soil development as observed in very old chronosequences. Moreover, our data show increases in soil organic carbon content and microbial biomass as soil develops that were negatively correlated with the abundance and diversity of soil ARGs. This work reveals natural dynamics of soil ARGs during pedogenesis and suggests that such ecological patterns are predictable, which together advances our understanding of the environmental drivers of ARGs in terrestrial environments.

Calling for comprehensive explorations between soil invertebrates and arbuscular mycorrhizas.

Arbuscular mycorrhizal (AM) fungi and soil invertebrates represent a large proportion of total soil biomass and biodiversity and are vital for plant performance, soil structure, and biogeochemical cycling. However, the role of soil invertebrates in AM fungi development remains elusive. In this opinion article, we summarize the ecological importance of AM fungi and soil invertebrates in the plant-soil continuum and highlight the effects of soil invertebrates on AM fungal hyphae development and functioning. In a context of global change, we envision that better mechanistic understanding of the complex feedback via chemical signaling pathways across the interactions between soil invertebrates and AM fungi is critical to predict their ecological consequences and will open new avenues for promoting ecosystem resilience and sustainability.

Climate warming increases the proportions of specific antibiotic resistance genes in natural soil ecosystems.

Understanding the future distribution of antibiotic resistance in natural soil ecosystems is important to forecast their impacts on ecosystem and human health under projected climate change scenarios. Therefore, it is critical and timely to decipher the links between climate warming and antibiotic resistance, two of Earth's most imminent problems. Here, we explored the role of five-year simulated climate warming (+ 4 °C) on the diversity and proportions of soil antibiotic resistance genes (ARGs) across three seasons in both plantation and natural forest ecosystems. We found that the positive effects of warming on the number and proportions of ARGs were dependent on the sampling seasons (summer, autumn and winter), and seasonality was a key factor driving the patterns of ARG compositions in forest soils. Fifteen ARGs, conferring resistance to common antibiotics including aminoglycoside, beta-lactam, macrolide-lincosamide-streptogramin B, multidrug, sulfonamide, and tetracycline, were significantly enriched in the warming treatment. We showed that changes in soil properties and community compositions of bacteria, fungi and protists can explain the changes in soil ARGs under climate warming. Taken together, these findings advance our understanding of environmental ARGs under the context of future climate change and suggest that elevated temperature may promote the abundance of specific soil ARGs, with important implications for ecosystem and human health.

The end of hunger: fertilizers, microbes and plant productivity.

It is a grand challenge to ensure the food security for a predicted world population of exceeding 9.7 billion by 2050, especially in an era of global climate change, land degradation and biodiversity loss. Current agricultural productions are mainly relying on synthetic chemical fertilisers to boost plant productivity but have undesirable effects on the environment and soil biodiversity. A promising direction in sustainable agriculture is to harness naturally occurring processes of beneficial plant-associated microbiomes to ensure sustained crop production and global food security. Despite the significant progress made in the development of beneficial microbes as inoculants to enhance plant performance, challenges remain with the translation of knowledge of plant and soil microbiomes to successful microbial products in the agricultural sector. Here, we highlight how fertilizer technology should be renovated by harnessing microbiome-based innovations to promote plant productivity and contribute to the end of hunger.

Livestock manure spiked with the antibiotic tylosin significantly altered soil protist functional groups.

With the increasing global antibiotic uses in livestock husbandry, animal manures upon land application pose potential threats to the environments and soil microbiome. Nevertheless, effects of manures and antibiotic-administered manures on soil protists, an integral component of soil food web and primary regulators of bacteria, remain unknown. Here, we assessed impacts of cattle and poultry manures with or without an antibiotic tylosin on soil protists and their functional groups in a 130-day microcosm incubation. Protists were highly responsive to manure application, with a significant decline in their alpha diversity in all manure treatments. There were also significant temporal changes in the alpha diversity and composition of soil protists and their functional groups. Poultry manures had stronger negative influences on the community structure of protists compared to cattle manures, and more pronounced effects on protists were observed in tylosin-spiked manure treatments. Furthermore, many consumer, phototrophic and parasitic taxa were highly susceptible to all manure treatments at Day 50 and 130. Altogether, our findings demonstrate negative effects of animal manures and tylosin on soil protists. This study suggests that the applications of livestock manures and antibiotics may subsequently alter ecological functions of protists and their interactions with other soil microorganisms in agricultural systems.