ISME Journal最新文献

Stresses (e.g., high temperature, drought, and pests) can reshape the structure of root-associated microbial communities, but how to discover functional microbial community assembly to support plant health remains a great challenge. Here we found that root-knot nematode (RKN) infection restructured the rhizosphere bacterial community in RKN-susceptible cucumber plants, regardless of the soil type. We isolated a Rhizobium pusense strain, TYQ1, which was significantly enriched following RKN infection. This strain not only directly inhibited RKNs but also caused the restructuring of the rhizobacterial community, thereby leading to the enrichment of multiple biomarker species. These enriched microorganisms, in collaboration with TYQ1, enhanced the biofilm-forming ability of the community and established a tightly interconnected metabolic interaction network, further strengthening the colonization of TYQ1 in the rhizosphere. Ultimately, the TYQ1-centered synthetic community exhibited more efficient and stable inhibition of RKNs. These findings highlight that stress-induced recruitment of keystone species can guide functional microbial community assembly to synergistically enhance plant health.

In the mutualism between leguminous plants and rhizobia bacteria, rhizobia live inside root nodules, creating potential for host genes to shape the rhizobial selective environment. Many host genes that affect symbiosis have been identified; however, the extent to which these genes affect selection acting on rhizobia is unknown. In this study, we inoculated 18 Medicago truncatula symbiotic mutants (including mutants that alter Nodule Cysteine-Rich (NCR) peptide production, plant defence, and nodule number regulation) with a mixture of 86 Sinorhizobium meliloti strains. Most mutations resulted in reduced host benefits, but the effects on rhizobial benefit (i.e., relative strain fitness) varied widely, revealing widespread host-by-strain fitness interactions. Genome-wide association analyses identified variants on rhizobial replicons pSymA and pSymB as important in mediating strain fitness responses to host mutations. Whereas most top variants affected rhizobial fitness with one host mutation (limited effect variants), nine affected fitness across six or more host mutations. These pervasive variants occurred primarily on pSymA, the symbiotic replicon, and include fixL and some metabolic genes. In contrast to the limited effect variants, variants with pervasive positive effects on strain fitness when host genes were mutated tended to adversely affect fitness in wild-type hosts. Competition assays across Medicago genotypes confirmed a pervasive role for one candidate (malonyl-CoA synthase), and AlphaFold multimer modelling suggests that many rhizobial top candidates could interact with host NCR peptides. Our results reveal how host genetic mutations alter strain fitness, setting the stage for improving rhizobial inoculants and breeding legume hosts better adapted to multi-strain environments.

Interspecies interactions can influence the physiology of competing species, shaping their long-term evolutionary trajectories. Although interspecific competition's role in community dynamics is well-documented, its impact on evolutionary outcomes and mechanisms is less explored. Here, we investigate how interspecies competition affects antibiotic resistance evolution in the gut pathogen Salmonella enterica within synthetic microbial communities. Specifically, we examine how the presence of an interspecific competitor, Escherichia coli, modulates resistance evolution at low streptomycin concentrations. Our findings reveal that interspecies competition results in the selection of S. enterica mutants with higher resistance levels by increasing the likelihood of accumulating resistance mutations that follow a trajectory of negative fitness epistasis. We show that this effect is driven by the enhanced expression of the cryptic aminoglycoside transferase gene (aadA). Our study thus links antibiotic resistance evolution to competition-induced physiological changes, emphasizing the interplay between interspecies interaction and adaptation to environmental conditions.

Marine microbes shape global biogeochemical cycles and marine food webs. Although biotic interactions underpin microbial community dynamics, most interactions between wild marine microbes are unknown. Here, we used empirical dynamic modeling to examine a six-year record of coastal microbial community composition to quantify microbial interactions and their changes through time. We found that, on average, marine microbes interact with 20% of other taxa in the community, most interactions are weak (80%), and that positive interactions are more common than negative interactions. Keystone taxa, defined as having disproportionally strong and frequent interactions, were not generally the most abundant taxa. The strength and sign of interactions, as well as the identity of the keystone taxa, varied through time and with changes in water temperature. An increase of 13°C, the dynamic range in water temperature at this location during the observational period, led to a 33% less interactive microbial community and an 11% shift towards more positive interactions. Only a few of the keystone taxa are the most interactive in the community at all times, and we found a temporal succession of keystone taxa. These results reveal that interactions in the marine microbiome are common, more facilitative than previously thought, and highly variable through time.

Microbes adopt diverse strategies to successfully compete with coexisting strains for space and resources. One common strategy is the production of toxic compounds to inhibit competitors, but the strength and direction of selection for this strategy vary depending on the environment. Existing theoretical and experimental evidence suggests that growth in spatially structured environments makes toxin production more beneficial because competitive interactions are localized. Because higher growth rates reduce the length scale of interactions in structured environments, theory predicts that toxin production should be especially beneficial under these conditions. We tested this hypothesis by developing a genome-scale metabolic modeling approach and complementing it with comparative genomics to investigate the impact of growth rate on selection for costly toxin production. Our modeling approach expands the current abilities of the dynamic flux balance analysis platform Computation Of Microbial Ecosystems in Time and Space (COMETS) to incorporate signaling and toxin production. Using this capability, we find that our modeling framework predicts that the strength of selection for toxin production increases as growth rate increases. This finding is supported by comparative genomics analyses that include diverse microbial species. Our work emphasizes that toxin production is more likely to be maintained in rapidly growing, spatially structured communities, thus improving our ability to manage microbial communities and informing natural product discovery.

Soil bacteria are prolific producers of a myriad of biologically active secondary metabolites. These natural products play key roles in modern society, finding use as anti-cancer agents, as food additives, and as alternatives to chemical pesticides. As for their original role in interbacterial communication, secondary metabolites have been extensively studied under in vitro conditions, revealing many roles including antagonism, effects on motility, niche colonization, signaling, and cellular differentiation. Despite the growing body of knowledge on their mode of action, biosynthesis, and regulation, we still do not fully understand the role of secondary metabolites on the ecology of the producers and resident communities in situ. Here, we specifically examine the influence of Bacillus subtilis-produced cyclic lipopeptides during the assembly of a bacterial synthetic community, and simultaneously, explore the impact of cyclic lipopeptides on B. subtilis establishment success in a synthetic community propagated in an artificial soil microcosm. We found that surfactin production facilitates B. subtilis establishment success within multiple synthetic communities. Although neither a wild type nor a cyclic lipopeptide non-producer mutant had a major impact on the synthetic community composition over time, both the B. subtilis and the synthetic community metabolomes were altered during co-cultivation. Overall, our work demonstrates the importance of surfactin production in microbial communities, suggesting a broad spectrum of action of this natural product.

Dinoflagellates are an abundant and diverse group of protists that inhabit aquatic environments worldwide. They are characterized by numerous unique cellular and molecular traits, and have adapted to an unusually broad range of life strategies, including phototrophy, heterotrophy, parasitism, and all combinations of these. For most microbial groups, transitions from marine to freshwater environments are relatively rare, as changes in salinity are thought to lead to significant osmotic challenges that are difficult for the cell to overcome. Recent work has shown that dinoflagellates have overcome these challenges relatively often in evolutionary time, but because this is mostly based on single gene trees with low overall support, many of the relationships between freshwater and marine groups remain unresolved. Normally, phylogenomics could clarify such conclusions, but despite the recent surge in data, virtually no freshwater dinoflagellates have been characterized at the genome-wide level. Here, we generated 30 transcriptomes from cultures and single cells collected from freshwater environments to infer a robustly supported phylogenomic tree from 217 conserved genes, resolving at least seven transitions to freshwater in dinoflagellates. Mapping the distribution of ASVs from freshwater environmental samples onto this tree confirms these groups and identifies additional lineages where freshwater dinoflagellates likely remain unsampled. We also sampled two species of Durinskia, a genus of "dinotoms" with both marine and freshwater lineages containing Nitzschia-derived tertiary plastids. Ribosomal RNA phylogenies show that the host cells are closely related, but their endosymbionts are likely descended from two distantly-related freshwater Nitzschia species that were acquired in parallel and relatively recently.

Accumulating evidence indicates that microorganisms respond to the ubiquitous plastic pollution by evolving plastic-degrading enzymes. However, the functional diversity of these enzymes and their distribution across the ocean, including the deep sea, remain poorly understood. By integrating bioinformatics and artificial intelligence-based structure prediction, we developed a structure- and function-informed algorithm to computationally distinguish functional polyethylene terephthalate-degrading enzymes (PETases) from variants lacking PETase activity (pseudo-PETase), either due to alternative substrate specificity or pseudogene origin. Through in vitro functional screening and in vivo microcosm experiments, we verified that this algorithm identified a high-confidence, searchable sequence motif for functional PETases capable of degrading PET. Metagenomic analysis of 415 ocean samples revealed 23 PETase variants, detected in nearly 80% of the samples. These PETases mainly occur between 1,000 and 2,000 m deep and at the surface in regions with high plastic pollution. Metatranscriptomic analysis further identified PETase variants that were actively transcribed by marine microorganisms. In contrast to their terrestrial counterparts-where PETases are taxonomically diverse-those in marine ecosystems were predominantly encoded and transcribed by members of the Pseudomonadales order. Our study underscores the widespread distribution of PETase-containing bacteria across carbon-limited marine ecosystems, identifying and distinguishing the PETase motif that underpins the functionality of these specialized cutinases.

Bacterial vaginosis (BV) is a common, polymicrobial condition of the vaginal microbiota that is associated with symptoms such as malodor and excessive discharge, along with increased risk of various adverse sequelae. Host-bacteria and bacteria-bacteria interactions are thought to contribute to the condition, but many of these functions have yet to be elucidated. Using untargeted metaproteomics, we identified 1068 host and 1418 bacterial proteins in a set of cervicovaginal lavage samples collected from 20 participants with BV and 9 who were negative for the condition. We identified Dialister micraerophilus as a major producer of malodorous polyamines and identified a syntrophic interaction between this organism and Fannyhessea vaginae that leads to increased production of putrescine, a metabolite characteristic of BV. Although formate synthesis has not previously been noted in BV, we discovered diverse bacteria associated with the condition express pyruvate formate-lyase enzymes in vivo and confirm these organisms secrete formic acid in vitro. Sodium hypophosphite efficiently inhibited this function in multiple taxa. We also found that the fastidious organism Coriobacteriales bacterium DNF00809 can metabolize formic acid secreted by Gardnerella vaginalis, representing another syntrophic interaction. We noted an increased abundance of the host epithelial repair protein transglutaminase 3 in the metaproteomic data, which we confirmed by enzyme-linked immunosorbent assay. Other proteins identified in our samples implicate Finegoldia magna and Parvimonas micra in the production of malodorous trimethylamine. Some bacterial proteins identified represent novel targets for future therapeutics to disrupt BV communities and promote vaginal colonization by commensal lactobacilli.

The source of protein in a person's diet affects their total life expectancy. However, the mechanisms by which dietary protein sources differentially impact human health and life expectancy are poorly understood. Dietary choices impact the composition and function of the intestinal microbiota that ultimately modulate host health. This raises the possibility that health outcomes based on dietary protein sources might be driven by interactions between dietary protein and the gut microbiota. In this study, we determined the effects of seven different sources of dietary protein on the gut microbiota of mice using an integrated metagenomics-metaproteomics approach. The protein abundances measured by metaproteomics can provide microbial species abundances, and evidence for the molecular phenotype of microbiota members because measured proteins indicate the metabolic and physiological processes used by a microbial community. We showed that dietary protein source significantly altered the species composition and overall function of the gut microbiota. Different dietary protein sources led to changes in the abundance of microbial proteins involved in the degradation of amino acids and the degradation of glycosylations conjugated to dietary protein. In particular, brown rice and egg white protein increased the abundance of amino acid degrading enzymes. Egg white protein increased the abundance of bacteria and proteins usually associated with the degradation of the intestinal mucus barrier. These results show that dietary protein sources can change the gut microbiota's metabolism, which could have major implications in the context of gut microbiota mediated diseases.