Niche separation in cross-feeding sustains bacterial strain diversity across nutrient environments and may increase chances for survival in nutrient-limited leaf apoplasts

The leaf microbiome plays a crucial role in plant's health and resilience to stress. Like in other hosts, successful colonization is dependent on multiple factors, among them, resource accessibility. The apoplast is an important site of plant-microbe interactions where nutrients are tightly regulated. While leaf pathogens have evolved elaborate strategies to obtain nutrients there, it is not yet clear how commensals survive without most of these adaptations. Resource limitation can promote metabolic interactions, which in turn shape and stabilize microbiomes but this has not been addressed in detail in leaves. Here, we investigated whether and how the nutrient environment might influence metabolic exchange and assembly of bacterial communities in Flaveria trinervia and F. robusta leaves. We enriched bacteria from both plant species in-vitro in minimal media with sucrose as a carbon source, and with or without amino acids. After enrichment, we studied the genetic and metabolic diversity within the communities. Enriched Pseudomonas koreensis strains could cross-feed from diverse leaf bacteria. Although P. koreensis could not utilize sucrose, cross-feeding diverse metabolites from Pantoea sp ensured their survival in the sucrose-only enrichments. The Pseudomonas strains had high genetic similarity (~99.8% ANI) but still displayed clear niche partitioning, enabling them to simultaneously cross-feed from Pantoea. Interestingly, cross-feeders were only enriched from F. robusta and not from F. trinervia. Untargeted metabolomics analysis of the leaf apoplasts revealed contrasting nutrient environments, with greater concentrations of high-cost amino acids in F. trinervia. Additionally, P. koreensis strains were better able to survive without a cross-feeding partner in these richer apoplasts. Thus, cross feeding might arise as an adaptation to cope with nutrient limitations in the apoplast. Understanding how apoplast resources influence metabolic interactions could therefore provide plant breeders targets to manipulate leaf microbiome shape and stability.

Mitochondrial Metabolism in Macrophages

Mitochondria are considered to be the powerhouse of the cell. Normal functioning of the mitochondria is not only essential for cellular energy production but also for several immunomodulatory processes. Macrophages operate in metabolic niches and rely on rapid adaptation to specific metabolic conditions such as hypoxia, nutrient limitations or reactive oxygen species to neutralize pathogens. In this regard, the fast reprogramming of mitochondrial metabolism is indispensable to provide the cells with the necessary energy and intermediates to efficiently mount the inflammatory response. Moreover, mitochondria act as a physical scaffold for several proteins involved in immune signaling cascades and their dysfunction is immediately associated with a dampened immune response. In this review, we put special focus on mitochondrial function in macrophages and highlight how mitochondrial metabolism is involved in macrophage activation.

Roles for Lo microdomains and ESCRT in ER stress-induced lipid droplet microautophagy in budding yeast

Microlipophagy (µLP), degradation of lipid droplets (LDs) by microautophagy, occurs by autophagosome-independent direct uptake of LDs at lysosomes/vacuoles in response to nutrient limitations and ER stressors in Saccharomyces cerevisiae. In nutrient-limited yeast, liquid-ordered (Lo) microdomains, sterol-rich raft-like regions in vacuolar membranes, are sites of membrane invagination during LD uptake. The endosome sorting complex required for transport (ESCRT) is required for sterol transport during Lo formation under these conditions. However, ESCRT has been implicated in mediating membrane invagination during µLP induced by ER stressors or the diauxic shift from glycolysis- to respiration-driven growth. Here, we report that ER stress induced by lipid imbalance and other stressors induces Lo microdomain formation. This process is ESCRT-independent and dependent upon Niemann-Pick type C sterol transfer proteins. Inhibition of ESCRT or Lo microdomain formation partially inhibits lipid imbalance-induced µLP, while inhibition of both blocks this µLP. Finally, although the ER stressors dithiothreitol or tunicamycin induce Lo microdomains, µLP in response to these stressors is ESCRT-dependent and Lo microdomain-independent. Our findings reveal that Lo microdomain formation is a yeast stress response, and stress-induced Lo microdomain formation occurs by stressor-specific mechanisms. Moreover, ESCRT and Lo microdomains play functionally distinct roles in LD uptake during stress-induced µLP.

Convergent evolution of a nutritional symbiosis in ants

Ants are among the most successful organisms on earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have repeatedly evolved symbioses to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Cardiocondyla, Formica and Plagiolepis ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine, which is essential for insect cuticles. We also reveal that in certain multi-queen lineages, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived nutrients. Our results suggest symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms.

Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem

Microbial communities display remarkable diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. Based on theoretical results indicating that cells can enhance their own growth rate by leaking even essential metabolites, we show that such “leaker” cells can establish an asymmetric form of mutualism with “consumer” cells that consume the leaked chemicals: the consumer cells benefit from the uptake of the secreted metabolites, while the leaker cells also benefit from such consumption, as it reduces the metabolite accumulation in the environment and thereby enables further secretion, resulting in frequency-dependent coexistence of multiple microbial species. As supported by extensive simulations, such symbiotic relationships generally evolve when each species has a complex reaction network and adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations. Accordingly, symbiotic ecosystems with diverse cell species that leak and exchange many metabolites with each other are shaped by cell-level adaptation of leakiness of metabolites. Moreover, the resultant ecosystems with entangled metabolite exchange are resilient against structural and environmental perturbations. Thus, we present a theory for the origin of resilient ecosystems with diverse microbes mediated by secretion and exchange of essential chemicals.