Carbon starvation raises capacities in bacterial antibiotic resistance and viral auxiliary carbon metabolism in soils.

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.

Nutrient status changes bacterial interactions in a synthetic community.

Microbial interactions affect community stability and niche spaces in all ecosystems. However, it is not clear what factors influence these interactions, leading to changes in species fitness and ecological niches. Here, we utilized 16 monocultures and their corresponding pairwise co-cultures to measure niche changes among 16 cultivable bacterial species in a wide range of carbon sources, and we used resource availability as a parameter to alter the interactions of the synthetic bacterial community. Our results suggest that metabolic similarity drives niche deformation between bacterial species. We further found that resource limitation resulted in increased microbial inhibition and more negative interactions. At high resource availability, bacteria exhibited little inhibitory potential and stronger facilitation (in 71% of cases), promoting niche expansion. Overall, our results show that metabolic similarity induces different degrees of resource competition, altering pairwise interactions within the synthetic community and potentially modulating bacterial niches. This framework may lay the basis for understanding complex niche deformation and microbial interactions as modulated by metabolic similarity and resource availability.IMPORTANCEUnderstanding the intricate dynamics of microbial interactions is crucial for unraveling the stability and ecological roles of diverse ecosystems. However, the factors driving these interactions, leading to shifts in species fitness and ecological niches, remain inadequately explored. We demonstrate that metabolic similarity serves as a key driver of niche deformation between bacterial species. Resource availability emerges as a pivotal parameter, affecting interactions within the community. Our findings reveal heightened microbial inhibition and more negative interactions under resource-limited conditions. The prevalent facilitation is observed under conditions of high resource availability, underscoring the potential for niche expansion in such contexts. These findings emphasize that metabolic similarity induces varying degrees of resource competition, thereby altering pairwise interactions within the synthetic community and potentially modulating bacterial niches. Our workflow has broad implications for understanding the roles of metabolic similarity and resource availability in microbial interactions and for designing synthetic microbial communities.

Assemblages of rhizospheric and root endospheric mycobiota and their ecological associations with functional traits of rice.

The soil-root interface harbors complex fungal communities that play vital roles in the fitness of host plants. However, little is known about the assembly rules and potential functions of rhizospheric and endospheric mycobiota. A greenhouse experiment was conducted to explore the fungal communities inhabiting the rhizosphere and roots of 87 rice cultivars at the tillering stage via amplicon sequencing of the fungal internal transcribed spacer 1 region. The potential relationships between these communities and host plant functional traits were also investigated using Procrustes analysis, generalized additive model fitting, and correlation analysis. The fungal microbiota exhibited greater richness, higher diversity, and lower structural variability in the rhizosphere than in the root endosphere. Compared with the root endosphere, the rhizosphere supported a larger coabundance network, with greater connectivity and stronger cohesion. Null model-based analyses revealed that dispersal limitation was primarily responsible for rhizosphere fungal community assembly, while ecological drift was the dominant process in the root endosphere. The community composition of fungi in the rhizosphere was shown to be more related to plant functional traits, such as the root/whole plant biomass, root:shoot biomass ratio, root/shoot nitrogen (N) content, and root/shoot/whole plant N accumulation, than to that in the root endosphere. Overall, at the early stage of rice growth, diverse and complex rhizospheric fungal communities are shaped by stochastic-based processes and exhibit stronger associations with plant functional traits. IMPORTANCE: The assembly processes and functions of root-associated mycobiota are among the most fascinating yet elusive topics in microbial ecology. Our results revealed that stochastic forces (dispersal limitation or ecological drift) act on fungal community assembly in both the rice rhizosphere and root endosphere at the early stage of plant growth. In addition, high covariations between the rhizosphere fungal community compositions and plant functional trait profiles were clearly demonstrated in the present study. This work provides empirical evidence of the root-associated fungal assembly principles and ecological relationships of plant functional traits with rhizospheric and root endospheric mycobiota, thereby potentially providing novel perspectives for enhancing plant performance.

Active microbial population dynamics and life strategies drive the enhanced carbon use efficiency in high-organic matter soils.

Microbial carbon use efficiency (CUE) is a critical parameter that controls carbon storage in soil, but many uncertainties remain concerning adaptations of microbial communities to long-term fertilization that impact CUE. Based on H218O quantitative stable isotope probing coupled with metagenomic sequencing, we disentangled the roles of active microbial population dynamics and life strategies for CUE in soils after a long-term (35 years) mineral or organic fertilization. We found that the soils rich in organic matter supported high microbial CUE, indicating a more efficient microbial biomass formation and a greater carbon sequestration potential. Organic fertilizers supported active microbial communities characterized by high diversity and a relative increase in net growth rate, as well as an anabolic-biased carbon cycling, which likely explains the observed enhanced CUE. Overall, these results highlight the role of population dynamics and life strategies in understanding and predicting microbial CUE and sequestration in soil.IMPORTANCEMicrobial CUE is a major determinant of global soil organic carbon storage. Understanding the microbial processes underlying CUE can help to maintain soil sustainable productivity and mitigate climate change. Our findings indicated that active microbial communities, adapted to long-term organic fertilization, exhibited a relative increase in net growth rate and a preference for anabolic carbon cycling when compared to those subjected to chemical fertilization. These shifts in population dynamics and life strategies led the active microbes to allocate more carbon to biomass production rather than cellular respiration. Consequently, the more fertile soils may harbor a greater microbially mediated carbon sequestration potential. This finding is of great importance for manipulating microorganisms to increase soil C sequestration.

Synthetic community derived from grafted watermelon rhizosphere provides protection for ungrafted watermelon against Fusarium oxysporum via microbial synergistic effects.

BACKGROUND: Plant microbiota contributes to plant growth and health, including enhancing plant resistance to various diseases. Despite remarkable progress in understanding diseases resistance in plants, the precise role of rhizosphere microbiota in enhancing watermelon resistance against soil-borne diseases remains unclear. Here, we constructed a synthetic community (SynCom) of 16 core bacterial strains obtained from the rhizosphere of grafted watermelon plants. We further simplified SynCom and investigated the role of bacteria with synergistic interactions in promoting plant growth through a simple synthetic community. RESULTS: Our results demonstrated that the SynCom significantly enhanced the growth and disease resistance of ungrafted watermelon grown in non-sterile soil. Furthermore, analysis of the amplicon and metagenome data revealed the pivotal role of Pseudomonas in enhancing plant health, as evidenced by a significant increase in the relative abundance and biofilm-forming pathways of Pseudomonas post-SynCom inoculation. Based on in vitro co-culture experiments and bacterial metabolomic analysis, we selected Pseudomonas along with seven other members of the SynCom that exhibited synergistic effects with Pseudomonas. It enabled us to further refine the initially constructed SynCom into a simplified SynCom comprising the eight selected bacterial species. Notably, the plant-promoting effects of simplified SynCom were similar to those of the initial SynCom. Furthermore, the simplified SynCom protected plants through synergistic effects of bacteria. CONCLUSIONS: Our findings suggest that the SynCom proliferate in the rhizosphere and mitigate soil-borne diseases through microbial synergistic interactions, highlighting the potential of synergistic effects between microorganisms in enhancing plant health. This study provides a novel insight into using the functional SynCom as a promising solution for sustainable agriculture. Video Abstract.

Ecology and risks of the global plastisphere as a newly expanding microbial habitat.

Plastic offers a new niche for microorganisms, the plastisphere. The ever-increasing emission of plastic waste makes it critical to understand the microbial ecology of the plastisphere and associated effects. Here, we present a global fingerprint of the plastisphere, analyzing samples collected from freshwater, seawater, and terrestrial ecosystems. The plastisphere assembles a distinct microbial community that has a clearly higher heterogeneity and a more deterministically dominated assembly compared to natural habitats. New coexistence patterns-loose and fragile networks with mostly specialist linkages among microorganisms that are rarely found in natural habitats-are seen in the plastisphere. Plastisphere microbiomes generally have a great potential to metabolize organic compounds, which could accelerate carbon turnover. Microorganisms involved in the nitrogen cycle are also altered in the plastisphere, especially in freshwater plastispheres, where a high abundance of denitrifiers may increase the release of nitrite (aquatic toxicant) and nitrous oxide (greenhouse gas). Enrichment of animal, plant, and human pathogens means that the plastisphere could become an increasingly mobile reservoir of harmful microorganisms. Our findings highlight that if the trajectory of plastic emissions is not reversed, the expanding plastisphere could pose critical planetary health challenges.