Protein is the main structural and functional component of cells, making it crucial for the survival of all living organisms. Yet mammalian herbivores and omnivores often consume diets deficient in the amount of protein required for growth, homeostasis, and reproduction. To compensate, mammals likely rely on their gut microbiota to synthesize essential amino acids (AAESS), particularly during periods of dietary protein limitation. We quantified the contribution of microbially synthesized AAESS to skeletal muscle in captive, wild-derived deer mice (Peromyscus maniculatus) fed diets varying in macromolecular quantity and quality. Using amino acid carbon isotope (δ13C) analysis combined with genetic sequencing, we assessed the origin of AAESS incorporated into host muscle and identified gut microbial taxa with the genetic potential for AAESS biosynthesis. We estimate that up to 25% of host muscle AAESS were microbially derived, with greater microbial contributions in mice fed diets containing low protein or more complex macronutrients. Gut microbial populations with the genetic potential for AAESS biosynthesis were more abundant in mice with larger contributions of microbially-derived AAESS in their tissues. These results demonstrate the crucial and likely pervasive role the gut microbiome plays in host protein metabolism, especially in mammals facing seasonal or persistent dietary protein limitation.

Antimicrobial resistance (AMR) poses a major threat to global human health. The emergence and spread of AMR is usually studied for single pathogen lineages. Therefore, we currently have only limited knowledge on the causes and dynamics of resistance evolution in polymicrobial or multistrain infections that involve different pathogen species or strains, respectively, even though these kinds of infections are widespread. To address these current knowledge gaps, we here used the opportunistic human pathogen Pseudomonas aeruginosa as a model to investigate how AMR evolves in populations with different genetically distinct strains (multistrain communities). By using controlled evolution experiments, extensive phenotyping and genome sequence analysis, we demonstrate that the response to antibiotic selection is shaped by a combination of strain-specific resistance profiles, ecological interactions between strains, and metapopulation structure. Moreover, the likelihood of de novo resistance evolution varied in dependence on mutation rates for resistance. A second independent evolution experiment emphasized the central role of strain variation and strain–strain interactions during adaptation. We conclude that AMR evolution in genetically diverse pathogen populations is driven by the interplay of ecological and evolutionary dynamics, thus deserving particular attention during treatment of polymicrobial infections.

Salinity strongly influences the physiology and distribution of nitrifying microorganisms, yet the effects of low salinity remain understudied. This study investigates the impact of hypoosmolarity on different groups of ammonia oxidizers in soil and freshwater reservoirs, as well as in pure culture isolates. In soil microcosms amended with ammonium, at low salinity levels (~120 μS/cm), comparable to values commonly found in pristine terrestrial and freshwater environments, the abundance of ammonia-oxidizing bacteria (AOB), dominated by Nitrosomonas oligotropha, significantly increased. In contrast, the growth of ammonia-oxidizing archaea (AOA), dominated by “Candidatus Nitrosotenuis” of the Nitrosopumilaceae family, was stimulated by high salinity (~760 μS/cm). In ammonium-fed freshwater microcosms, the abundance of AOB, dominated by N. oligotropha, significantly increased under both low (~170 μS/cm) and high salinity (~850 μS/cm) conditions. In the presence of allylthiourea (50 μM), used to inhibit bacterial ammonia oxidation, AOA were sensitive to low salinity in both soil and freshwater microcosms. Consistently, culture-dependent studies revealed marked growth inhibition of terrestrial AOA, especially members of Nitrosopumilaceae, under hypoosmolarity, unlike AOB and complete ammonia oxidizer (comammox) strains. Genomic analyses, along with transcriptomic studies, suggested that the sensitivity of AOA to hypoosmolarity stress was possibly due to a lack of osmoregulatory transport systems and their S-layer cell wall structure. Overall, this study indicates hypoosmolarity as an important factor shaping the ecological niches and distribution of ammonia oxidizers, as well as nitrification activities, in terrestrial and freshwater environments that are increasingly affected by intensified water cycles due to global change.

The bodies of macroorganisms host microbes living in multispecies communities. Sequencing approaches have revealed that different organs host different microbiota and tend to be infected by different pathogens, drawing correlations between environmental parameters at the organ level and microbial composition. However, less is known about the microscale dimension of microbial ecology, particularly during infection. In this study, we focus on the role of microscale spatial structure, studying its influence on the ecology of a polymicrobial infection of Pseudomonas aeruginosa, Staphylococcus aureus, and Candida albicans. Although these pathogens are commonly found together in the lungs of chronically ill patients, it is unclear whether they coexist or compete and segregate in different niches. We find that, whereas P. aeruginosa quickly outcompetes C. albicans and S. aureus on large surfaces, robust spatial organization and coexistence emerges in spatially structured microenvironments. In confined spaces, slowly growing C. albicans is able to leverage rapid radial hyphal growth to conquer boundaries, where it establishes itself displacing the other pathogens. Similar outcomes are observed when the P. aeruginosa strain carries mexT-inactivating mutations, which are often found in clinical isolates. The observed spatial organization enables coexistence and potentially determines infection severity and outcomes. Our findings reveal a previously unrecognized role of mechanical forces in shaping infection dynamics, suggesting that microenvironmental structure might be a critical determinant of pathogen coexistence, virulence, and treatment outcomes. Because adaptations, such as changes in morphology, are widespread among microbes, these results are generalizable to other ecologies and environments.

Bacterial-fungal interactions have traditionally been attributed to secondary metabolites, but the role of the bacterial extracellular matrix in shaping these relationships has remained unclear. Here, we demonstrate that the extracellular matrix protein TasA is a key mediator in the antagonistic interaction between Bacillus subtilis and Botrytis cinerea. TasA enables Bacillus to tightly adhere to fungal hyphae, disrupts the β-glucan layer, and compromises fungal cytoskeletal integrity synergistically with fengycin, which causes cytological damage. Additionally, TasA acts as a carrier for bacillaene, amplifying its fungistatic activity. In response, Botrytis mounts a multifaceted defense, enzymatically degrading fengycin, producing antibacterial oxylipins, and activating adaptive programs such as hyphal branching and chlamydospore formation. Our findings reveal the previously unrecognized role of extracellular matrix components in fungal suppression and the modulation of fungal adaptive responses. This study reveals the complex interplay between microbial aggression and defense, providing new insights into the ecological dynamics of microbial competition and coexistence.

The hadal trenches, the deepest regions of the ocean, serve as the final sinks for marine particles and "tunnels" for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trench sediments contain high content of organic carbon and active microbial carbon turnover, are hotspots for deep-sea organic carbon degradation and unique microbial processes. However, little is known about the organic carbon components and microbial metabolisms driving their degradation in trench sediments. This study provides the first comprehensive quantification of total halogenated organic compounds (organohalides) in Mariana Trench sediments. The measured bulk organic halogen concentrations exceeded all previously reported individual compounds by orders of magnitude, with a mean stoichiometric ratio of 1:49 (halogen:carbon) in the sedimentary organic carbon pool. These findings suggest the trench sediments may represent a significant reservoir for organohalides. Metagenomic analysis of global ocean data shows significant enrichment of the genes for organohalides biodegradation (dehalogenation) in trench microbiomes than those in other marine environments. Putative dehalogenating microorganisms in trench sediments encompassed 16 phyla and 52 orders, capable of metabolizing 18 structurally diverse organohalide compounds, revealing an unexpectedly broad phylogenetic distribution of organohalides metabolism and versatile substrate specificity among trench microbial communities. High pressure microcosm experiments demonstrated rapid degradation of typical organohalide compounds and transcription of genes related to organohalides metabolisms, confirming an active organohalides degradation by trench microorganisms. These findings underscore the role of organohalides metabolism in organic carbon remineralization in hadal trenches, advancing our understanding of deep-sea carbon cycling and microbial survival.

Coral reef ecosystems rely on microorganisms to carry out biogeochemical processes essential to the survival of corals and the reef food web. However, widespread shifts from coral to algal dominance as a result of anthropogenic pressures have promoted microbial communities that compromise reef health through deoxygenation and disease. These degraded reefs become locked in a “microbialized” state characterized by high microbial biomass, low oxygen, and heightened pathogenic activity that stymie efforts to outplant corals onto the reef, a common approach applied to restore these ecosystems. Over 18 months, we compared viral and microbial dynamics alongside physical and chemical parameters (“water quality”) between two coral outplanting sites and two midwater reef mesocosms called Coral Arks. Seafloor sites exhibited microbialization, whereas Arks maintained conditions with higher viral abundances and virus-to-microbe ratios, smaller and less abundant microorganisms, and consistently higher dissolved oxygen, water flow, and light availability. These conditions, which we term “viralized”, supported enhanced coral growth and survival, greater benthic diversity, increased coral recruitment, reduced turf and macroalgae, and higher fish abundance compared to outplanting sites. Despite these benefits, analysis of microbial carbon metabolism genes revealed an underlying trend towards microbialization at both sites, reflecting larger-scale regional decline. These findings emphasize that microbial and physicochemical conditions are drivers of reef restoration outcomes; to be successful, restoration strategies must target the underlying environmental factors that support coral survival and resilience. We identify key microbial and physical variables—such as oxygen levels, flow, and viral activity—associated with viralized reef states, which should serve as focal points for developing new interventions and technologies aimed at creating conditions conducive to reef recovery.

Global environmental change substantially affects soil detritivores, including earthworms, impacting host-microbiota interactions and altering key soil biogeochemical processes such as litter decomposition. As microbial communities are inherently capable of rapid evolution, responses of earthworms and associated microbiota (i.e. earthworm holobionts) to global environmental change may likely involve the interplay of ecological and evolutionary processes and feedback. Although species-level responses of earthworms to global environmental change are well studied, the potential ecological and evolutionary responses of earthworm holobionts to environmental change remain unexplored. Here, we provide a conceptual framework to elaborate on the complex network of earthworm host-microbiota interactions that modify their traits in response to global environmental change, jointly shaping their ecology and evolution. Based on the literature, we synthesize evidence of global environmental change impacts on earthworm host-microbiota and discuss evidence of their ecological and evolutionary responses to environmental change. Lastly, we highlight the agro- and eco-system-level consequences of environmental change-mediated shift in earthworm host-microbiota functions. Soil legacies of environmental change have cascading detrimental impacts on the abundance, diversity, and functional dynamics of earthworm host-microbiota interactions in agriculture and ecosystems. The primary mechanisms driving such responses of earthworm hosts and associated microbial communities to environmental change include altered litter quality and host dietary preferences, competitive interactions and exclusion, habitat homogenization, and a shift in soil physicochemical and biological processes. Therefore, advancing knowledge of the intricate animal-microorganism interactions is crucial for belowground biodiversity management in a changing global environment.

The diffusible toxin ColIb produced by Salmonella enterica serovar Typhimurium SL1344 is a potent inhibitor of Escherichia coli growth. To identify and parameterize metabolic cross-feeding in states of competition, we established defined communities in which E. coli was the only species able to access a sole carbon source, lactose. Although ColIb was predicted to undermine cross-feeding by killing the lactose-converting E. coli, S. enterica populations thrived in co-culture. We discovered that ColIb caused the release of active β-galactosidase from E. coli cells, which induced galactose uptake by S. enterica. Although iron limitation stimulates ColIb production and makes E. coli more sensitive to the toxin, ColIb killing in iron-limited conditions did not enhance iron acquisition or siderophore scavenging by S. enterica. Also unexpected was the rapid rate at which resistance to ColIb evolved in E. coli through spontaneous mutation of the ColIb receptor gene cirA or horizontal acquisition of the S. enterica colicin immunity gene imm. Mathematical modelling effectively predicted the growth kinetics of E. coli and S. enterica populations, revealing a tractable system in which ColIb can shrink a competitor population while simultaneously amplifying the metabolic contributions of the suppressed population.

Understanding how microbial communities maintain stable compositional diversity is a key question in microbial ecology. Studies from pairwise interactions and synthetic communities indicate that metabolic interactions and spatial organisation can influence diversity, but the relevance of these factors in more complex communities is unclear. Here we used a cyanobacterial enrichment community that consistently forms millimetre-scale granular structures, to investigate compositional diversity and its stability. Over a year of passaging in media without significant carbon source, we found stable co-existence of 17 species belonging to diverse bacterial phyla. Metagenomic analysis revealed polysaccharide breakdown genes and complementary vitamin biosynthesis pathways in these species. Supporting these findings, we show growth of several isolated species on cyanobacterial slime components and experimentally verify vitamin exchanges between two members of the community. Several species had genes for (an)oxygenic photosynthesis and sulfur cycling, the expression of which we verified via metatranscriptomics. Consistent with this, we found that the granular structures displayed oxygen gradients with anoxic interiors. Cyanobacteria and other bacteria were distributed on the periphery and insides of these structures, respectively. Perturbation of the community via glucose addition resulted in fold increases of the heterotrophs, whereas disturbing the community by continual shaking led to fold reductions in several heterotrophs, including anoxygenic phototrophs. In contrast, removal of vitamins supplementation did not consistently alter species coverages, due to predicted vitamin sharing amongst community members. Taken together, these findings indicate that spatial organisation, microenvironment niche formation and metabolic interactions contribute to community compositional diversity and stability.