Microbial volatiles mediate bacterial evolutionary dynamics
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Community composition and physiological plasticity control microbial carbon storage across natural and experimental soil fertility gradients
Many microorganisms synthesise carbon (C)-rich compounds under resource deprivation. Such compounds likely serve as intracellular C-storage pools that sustain the activities of microorganisms growing on stoichiometrically imbalanced substrates, making them potentially vital to the function of ecosystems on infertile soils. We examined the dynamics and drivers of three putative C-storage compounds (neutral lipid fatty acids [NLFAs], polyhydroxybutyrate [PHB], and trehalose) across a natural gradient of soil fertility in eastern Australia. Together, NLFAs, PHB, and trehalose corresponded to 8.5–40% of microbial C and 0.06–0.6% of soil organic C. When scaled to “structural” microbial biomass (indexed by polar lipid fatty acids; PLFAs), NLFA and PHB allocation was 2–3-times greater in infertile soils derived from ironstone and sandstone than in comparatively fertile basalt- and shale-derived soils. PHB allocation was positively correlated with belowground biological phosphorus (P)-demand, while NLFA allocation was positively correlated with fungal PLFA : bacterial PLFA ratios. A complementary incubation revealed positive responses of respiration, storage, and fungal PLFAs to glucose, while bacterial PLFAs responded positively to PO43-. By comparing these results to a model of microbial C-allocation, we reason that NLFA primarily served the “reserve” storage mode for C-limited taxa (i.e., fungi), while the variable portion of PHB likely served as “surplus” C-storage for P-limited bacteria. Thus, our findings reveal a convergence of community-level processes (i.e., changes in taxonomic composition that underpin reserve-mode storage dynamics) and intracellular mechanisms (e.g., physiological plasticity of surplus-mode storage) that drives strong, predictable community-level microbial C-storage dynamics across gradients of soil fertility and substrate stoichiometry.
The mechanism effects of root exudate on microbial community of rhizosphere soil of tree, shrub, and grass in forest ecosystem under N deposition
Forests are composed of various plant species, and rhizosphere soil microbes are driven by root exudates. However, the interplay between root exudates, microbial communities in the rhizosphere soil of canopy trees, understory shrubs, grasses, and their responses to nitrogen (N) deposition remains unclear. Pinus tabulaeformis, Rosa xanthina, and Carex lancifolia were used to investigate root exudates, rhizosphere soil microbial communities, and their responses to N application in forest ecosystem. Root exudate abundances of P. tabulaeformis were significantly higher than that of R. xanthina and C. lancifolia, with carbohydrates dominating P. tabulaeformis and R. xanthina root exudates, fatty acids prevailing in C. lancifolia root exudates. Following N application, root exudate abundances of P. tabulaeformis and R. xanthina initially increased before decreasing, whereas those of C. lancifolia decreased. Microbial number of rhizosphere soil of C. lancifolia was higher than that of P. tabulaeformis and R. xanthina, but there was insignificant variation of rhizosphere soil microbial diversity among plant species. N application exerted promotional and inhibitory impacts on bacterial and fungal numbers, respectively, while bacterial and fungal diversities were increased by N application. Overall, N application had negative effects on root exudates of P. tabulaeformis, inhibiting rhizosphere soil microbial populations. N application suppressed rhizosphere soil microbial populations by increasing root exudates of R. xanthina. Conversely, N application elevated nutrient content in the rhizosphere soil of C. lancifolia, reducing root exudates and minimally promoting microbial populations. This study highlights the importance of understory vegetation in shaping soil microbial communities within forests under N deposition.
Microbial phosphorus recycling in soil by intra- and extracellular mechanisms
Rising global stoichiometric imbalance between increasing nitrogen (N) availability and depleting phosphorus (P) resources increases the importance of soil microbial P recycling. The contribution of extra- versus intracellular P (re-)cycling depending on ecosystem nutrient status is vastly unclear, making soil microorganisms a blind spot in our understanding of ecosystem responses to increasing P deficiency. We quantified P incorporation into microbial DNA and phospholipids by 33P labeling under contrasting conditions: low/high P soil × low/high carbon (C)NP application. By combining 33P and 14C labeling with tracing of microbial community biomarkers and functional genes, we disengaged the role of DNA and phospholipids in soil P cycling. Microorganisms in low P soil preferentially allocated P to phospholipids with an acceleration of phospholipids metabolism driven by C addition, which was strongly related to high abundances of microbial community members (e.g. some G-) with a fast phospholipids turnover. In high P soil, however, more P was allocated to DNA with a microbial functional shift towards DNA synthesis to support a replicative growth when sufficient C was supplied, which was coupled with a strong enrichment of fungal copiotrophs and microbial genes coding DNA primase. Consequently, adaptation to low P availability accelerated microbial intracellular P recycling through reutilization of the P stored in phospholipids. However, microorganisms under high P availability commonly adopted extracellular P recycling with release and reuse of DNA P by microbial death-growth dynamics. These results advance our understanding on microbial adaptation to P deficiency in soil by regulating component-specific P pathways and reflect the specific functions of phospholipids and DNA for P recycling.
High intensity perturbations induce an abrupt shift in soil microbial state
Soil microbial communities play a pivotal role in regulating ecosystem functioning. But they are increasingly being shaped by human-induced environmental change, including intense “pulse” perturbations, such as droughts, which are predicted to increase in frequency and intensity with climate change. While it is known that soil microbial communities are sensitive to such perturbations and that effects can be long-lasting, it remains untested whether there is a threshold in the intensity and frequency of perturbations that can trigger abrupt and persistent transitions in the taxonomic and functional characteristics of soil microbial communities. Here we demonstrate experimentally that intense pulses of drought equivalent to a 30-year drought event (<15% WHC) induce a major shift in the soil microbial community characterised by significantly altered bacterial and fungal community structures of reduced complexity and functionality. Moreover, the characteristics of this transformed microbial community persisted after returning soil to its previous moisture status. As a result, we found that drought had a strong legacy effect on bacterial community function, inducing an enhanced growth rate following subsequent drought. Abrupt transitions are widely documented in aquatic and terrestrial plant communities in response to human-induced perturbations. Our findings demonstrate that such transitions also occur in soil microbial communities in response to high intensity pulse perturbations, with potentially deleterious consequences for soil health.
Microbial gene expression analysis of healthy and cancerous esophagus uncovers bacterial biomarkers of clinical outcomes
Local microbiome shifts are implicated in the development and progression of gastrointestinal cancers, and in particular, esophageal carcinoma (ESCA), which is among the most aggressive malignancies. Short-read RNA sequencing (RNAseq) is currently the leading technology to study gene expression changes in cancer. However, using RNAseq to study microbial gene expression is challenging. Here, we establish a new tool to efficiently detect viral and bacterial expression in human tissues through RNAseq. This approach employs a neural network to predict reads of likely microbial origin, which are targeted for assembly into longer contigs, improving identification of microbial species and genes. This approach is applied to perform a systematic comparison of bacterial expression in ESCA and healthy esophagi. We uncover bacterial genera that are over or underabundant in ESCA vs healthy esophagi both before and after correction for possible covariates, including patient metadata. However, we find that bacterial taxonomies are not significantly associated with clinical outcomes. Strikingly, in contrast, dozens of microbial proteins were significantly associated with poor patient outcomes and in particular, proteins that perform mitochondrial functions and iron-sulfur coordination. We further demonstrate associations between these microbial proteins and dysregulated host pathways in ESCA patients. Overall, these results suggest possible influences of bacteria on the development of ESCA and uncover new prognostic biomarkers based on microbial genes. In addition, this study provides a framework for the analysis of other human malignancies whose development may be driven by pathogens.
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