搜索结果：The ISME journal

As a prevalent congener of polybrominated diphenyl ethers (PBDEs), 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) poses significant environmental and health risks due to its persistence and bioaccumulation. However, the limited understanding of the microbial degradation mechanism of BDE-47 has hindered the development of effective bioremediation strategies. Here, we decipher an aerobic catabolic pathway of BDE-47 mediated by metabolic relay within a synthetic consortium composed of two environmental isolates, Rhizorhabdus wittichii YL-JM2C and Cupriavidus necator JMP134. Bioaugmentation with this consortium achieved complete removal of BDE-47 in real wastewater samples. The molecular basis underlying this cooperative degradation was elucidated through the heterologous expression and functional characterization of key enzymes involved. Namely, the dioxygenase TcsAaAb from strain YL-JM2C catalyzed the initial conversion of BDE-47 into 2,4-dibromophenol (2,4-DBP) and 3,5-dibromocatechol (3,5-DBC). As a dead-end intermediate in strain YL-JM2C, the former (2,4-DBP) was subsequently transformed into the latter (3,5-DBC) by the hydroxylase TfdB from strain JMP134. The resulting 3,5-DBC was catabolized through the downstream ortho-cleavage pathway present in both strains. These key enzymes for BDE-47 degradation coexist across diverse environments, including soil, seawater, and marine sediments. Global marine metagenomic profiling revealed a significant enrichment of these catabolic signatures in the Mariana Trench, implying that microorganisms in the hadal zone possess the genetic potential for PBDE catabolism. This study unveils previously unrecognized aerobic catabolic mechanisms for BDE-47 within natural ecosystems, offering promising bioremediation strategies for PBDE-contaminated environments.

The Lactobacillaceae inhabit diverse environments, but the extent of their habitat adaptation remains unclear and the colonization factors unknown. First, we applied multiple machine learning models to determine if we can distinguish strains of the same species isolated from two different habitats based on their gene content. Surprisingly, we show that no species is differentially adapted to the oral cavity versus the human gut, or food versus the human gut, while only Lactobacillus crispatus showed specialization to the human urogenital system versus human gut. We then asked which species of Lactobacillaceae are habitat-specialized and how they could be identified. Using multiple lifestyle predictors incorporated in logistic regression models, we found that Limosilactobacillus reuteri, Ligilactobacillus ruminis, Ligilactobacillus salivarius, L. crispatus, and Limosilactobacillus mucosae displayed the highest degrees of host specialization. Applying our microbial genome-wide association study tool, aurora, to these species identified genes encoding adhesins and bacteriocins as the strongest and most common adaptation factors. This work establishes a generalizable framework for identifying novel species-habitat pairs with strong evidence of specialization and for uncovering the genomic features underlying within-species host and habitat adaptation.

Bacterial extracellular vesicles (BEVs) are nanoscale membranous structures released by diverse types of bacteria, and are capable of transporting and delivering biological compounds between cells. Experimental investigation of BEVs in laboratory model systems indicates that these nanoparticles may play a number of roles in the ecophysiology of marine bacterial communities, but their functional potential in the environment remains unclear. Here we describe the proteomic composition of BEV populations over more than 5000 nautical miles of surface waters in the South Pacific, linking BEV cargoes to the bacterial communities producing them. The presence of marine BEVs was consistently observed across a range of biogeochemical conditions, with an overall abundance comparable to that of bacterial cells (up to 108 BEVs L-1). The protein cargo of marine BEVs, however, differed significantly among ocean regions. The BEV populations were enriched in carbohydrate transporters under phytoplankton bloom conditions, and contained iron uptake-related proteins in nutrient-limited waters. These data suggest that BEVs could enable cells to perform key extracellular functions in the marine environment. Our observations highlight the ubiquity of marine BEVs and biogeographic patterns in their ecological potential across oceanic scales.

Insertion sequences (ISs) are widespread prokaryotic transposable elements, often regarded as genomic parasites that primarily cause deleterious mutations. However, they can also promote adaptive changes. These antagonistic properties make their overall impact on prokaryotic evolution difficult to grasp. Here, we address this challenge by leveraging the framework of transposon ecology to analyze IS occurrences across and within 30,499 prokaryotic genomes. Combining phylogenomics with multi-scale genomic analysis, quantitative ecology, and mathematical modeling, we provide evidence that although genomes generally provide sufficient resources for IS coexistence, universal mechanisms shape their occurrence and chromosomal distribution across genomes. These include: (i) the preferential localization of ISs within highly variable and GC-heterogeneous chromosomal regions of genomic plasticity (RGPs), which act as the primary reservoir of IS niches; (ii) a linear scaling between IS abundance and niche size, with an average of $5.4$ additional accessible insertion sites per IS; (iii) a dependence of IS occurrence on the presence of other ISs, suggesting a form of group behavior; (iv) the accumulation of AT-rich sequences in both coding and non-coding regions up to 100 kb surrounding ISs, indicative of ecological isolation; and (v) the spatial partitioning of mobile genetic elements around ISs, reminiscent of ecological niche differentiation. Besides these general principles, we also uncover niche specificities associated with particular IS families, hinting at regulatory mechanisms that modulate IS activity. Altogether, this comprehensive transposon ecology approach offers new insights and avenues for understanding IS-host interactions and genome evolution, moving beyond traditional host-centric perspectives.

Bulk microbiome analysis obscures the spatial heterogeneity of microbial communities, limiting the understanding of bacterial distribution inside fungal sclerotia, which are the survival structures of the plant pathogen Sclerotinia sclerotiorum. Although studies have profiled microbiomes of different fungal structures, sclerotia microbiome remains largely unexplored. We applied bulk microbiome using PacBio full-length 16S rRNA sequencing, synthetic community (SynCom), and 10x Genomics Xenium platform to resolve the spatiotemporal contribution of soil bacteria to sclerotia mortality. In the bulk microbiome, the relative abundance of soil bacteria such as Massilia and Trinickia were enriched when sclerotia mortality increased under flooding conditions. Twelve enriched sclerotia-associated bacteria were assembled into a SynCom to study their causality for sclerotia mortality. Spatial microbiome analysis revealed the temporal dynamics and distribution pattern of each SynCom member. Among them, Trinickia sclerotiorum sp. nov. type strain MC (TsMC) was found to reach the most interior sclerotia and its relative abundance coincided with sclerotia mortality. TsMC exhibits the highest importance in four antagonistic assays and SynCom drop-out test. Whole genome sequencing confirmed TsMC as a novel species with antifungal potentials. Collectively, we document a novel bacterium for sclerotia mortality and demonstrate the advantage of spatiotemporal distribution in microbiome research.

Cobamides, including vitamin B12, are essential cofactors exchanged between organisms across diverse ecosystems including oceans, soils, and the mammalian gut. Although most organisms depend on cobamides, only a minority of prokaryotes perform their metabolically costly biosynthesis. This has led to vitamin B12 uptake from the environment as a common acquisition strategy, but does not explain why B12 producers would allow B12 to become extracellularly available. Our work reconciles this inconsistency, showing that bacteriophages (phages) can facilitate the release of intracellular B12 at physiologically relevant concentrations. Phages are viruses that infect and often lyse their targeted bacteria, which may externalize intracellular material along with progeny phages. In this work, we aimed to determine whether phage-mediated lysis promotes the externalization of vitamin B12, thereby supporting the growth of B12-dependent bacteria. To test this, we first used genetically well-defined B12-Producer and B12-User bacteria, and found that phage-mediated lysis of the producers releases sufficient B12 to support the growth of the users in co-culture. Next, we showed that phage-mediated lysis of the B12-producer can similarly support the growth of various commensal gut bacteria that are also B12-dependent, in co-culture. B12 released by phage-mediated cell lysis induced significant compositional changes among the non-targeted bacteria including an increased diversity that was muted by supplementing B12 in the medium. Collectively, these findings suggest that phage-mediated bacterial lysis is a significant contributor to nutrient externalization in microbial communities, leading to broad compositional changes beyond their host range.

Yeasts are prevalent members of the phyllosphere microbiome, but fundamental knowledge of the chemical basis of their interactions with other members of the phyllosphere microbiota remains largely elusive. Our previous study revealed that wheat flag leaves harbor taxonomically diverse populations of yeasts with various traits important for successful colonization and survival in the harsh phyllosphere environment. In this study, we investigated interactions between two specific yeast genera, Aureobasidium and Metschnikowia, and the mycotoxigenic fungus Fusarium graminearum, causal agent of Fusarium head blight (FHB). Using multiple experimental approaches, we demonstrate that phyllosphere yeasts effectively colonize wheat leaves and heads, markedly reducing FHB incidence when established before pathogen arrival. Based on metabolomic data, we further show that Aureobasidium and Metschnikowia isolates can degrade the Fusarium mycotoxin deoxynivalenol (DON) and DON-inducing plant compounds produced during or in response to FHB. Our findings highlight the ecology of phyllosphere yeasts and the chemical basis of their multipartite interactions with a mycotoxigenic fungus and the host plant.

Chlamydomonas reinhardtii is a unicellular green alga long studied as a biological model system but rarely considered from the perspective of its own ecology, thus epitomizing the disconnection between reductionist biology in the laboratory and life in nature. Here we present insights into its ecology understood from field strains. We examined bacterial communities that coenriched with C. reinhardtii from the field, revealing specific associations. We then compared the biology of C. reinhardtii field strains to laboratory strains, illuminating strain level heterogeneity and adaptations to life in the field vs. laboratory. Field strains exhibited more robust photosynthesis, higher abundances of pherophorin proteins, a propensity for pallmeloid formation, and high cell wall permeability. Finally, we phenotyped cocultures of C. reinhardtii with a coenriched bacterial partner, demonstrating how differences between field and laboratory strains manifest in biotic interactions. Although the organisms in question are classically understood as unicellular, our observations of field strains highlighted their participation in multicellular units, challenging the utility of unicellular frameworks in extending our knowledge of model organism biology in the laboratory towards understanding microbial ecology.

Extracellular superoxide generated by heterotrophic bacteria influences aquatic redox transformations, yet its regulation within the phycosphere remains poorly understood. Here, we show that the cyanobacterium Microcystis aeruginosa enhances extracellular superoxide production by Pseudomonas sp. QJX-1 under illumination. Cocultivation increased extracellular superoxide production approximately three-fold over bacterial monoculture, with maximum enhancement during carbon starvation. Membrane separation localized detectable superoxide production to the bacterial chamber, indicating that diffusible algal products stimulated bacterial superoxide production. Mechanistically, illuminated cocultures showed 20.4% higher photocurrent than algal monocultures and accumulated the highest extracellular NADP(H) levels, indicating intensified photosynthesis-associated extracellular redox activity. Reduced nicotinamide cofactors stimulated diphenyleneiodonium-sensitive QJX-1-associated superoxide production, consistent with an oxidoreductase-associated route for one-electron reduction of molecular oxygen. In parallel, coculture accumulated catecholate siderophores, consistent with intensified microscale Fe competition; this siderophore-enhanced response required metabolically active bacterial cells and was attenuated by respiratory-chain inhibition. Representative extracellular redox-active and algal photoactive components further enhanced the bacterial response, with cytochrome c and chlorophyll a stimulating QJX-1-associated superoxide production under defined conditions. Functionally, during the carbon-starvation interval coinciding with peak superoxide production, the apparent sulfamethoxazole removal rate constant in coculture was 2.6 times that observed for QJX-1 alone. Moreover, quenching extracellular reactive oxygen species (ROS) impaired metabolic activity under diverse chemical stressors and reduced carbon, nitrogen, and phosphorus substrate utilization. Collectively, these findings identify photosynthesis-dependent phycosphere interactions as regulators of bacterial superoxide production, linking biogenic ROS to contaminant transformation, chemical-stress resilience, and elemental nutrient turnover.

We propose a suite of simple equations to estimate the probability and duration of two important processes in microbial ecology: immigration and extinction. Our work is based on the gambler's ruin equation, which determines the probability that a number of immigrants (i) can attain an abundance N given the ratio of the probabilities of death q and division (or birth) p. We estimate the probability of an organism attaining a value of N in the context of bioaugmentation, transplantation, infection, mutation, and extinction. For example, an inoculum of 108 bacteria with a q/p of 1.00000001 has a 10-43 chance of attaining an abundance of 1010. The ratio of deaths to births controls the immigration parameter used in neutral models (m), and infectious dose in pathogens. We use Vibrio cholerae infections to demonstrate that the gambler's ruin equation can be used to estimate the infectious dose in naturally occurring infections. We calculated the long-term average value of m and q/p in a wastewater treatment plant. All values of q/p were ≥1. We expect the long-term average value of q/p to be ~1 in all stable microbial communities. In the absence of migration, bacterial populations with q/p ≥1 will go extinct with probability 1. We use the ratio q/p and simple recurrence relationships to estimate the time for a given change in abundance to occur. When q/p=1, extinction in even a small microbial population will take thousands of years. Our simple mechanistic models could play a powerful role in theory and practice.

Microbial populations strongly shape their environment, which can re-route adaptation toward organism-generated fitness optima. However, the conditions that promote these eco-evolutionary feedbacks are unclear. Here, we used experimental evolution to test whether high population density, by strengthening niche construction, drives eco-evolutionary feedbacks in the bacterial pathogen Pseudomonas aeruginosa MPAO1. We then tested for adaptation to organism-modified environments by measuring the relative performance of ancestral and endpoint populations in filtrate generated by each evolutionary line sampled across generations. Contrary to expectations, we found that endpoint populations had higher performance than the ancestral strain in filtrate across nearly all evolutionary lines regardless of population density. This was caused by the emergence of hyperactive filamentous bacterio(phage) mutants during experimental passaging that inhibited the ancestral strain but not endpoint populations in modified media. Hyperactive phages emerged from one of two avirulent prophages in MPAO1's genome (Pf4 or Pf6). Hyperactive phages drove the evolution of phage resistance in bacterial populations via mutations in the type IV pilus (TIVP), the phage's binding receptor. In a follow-up experiment, we showed that these TIVP mutations pleiotropically reduced motility and decreased susceptibility to a TIVP-targeting virulent phage, both of which are important traits for P. aeruginosa infection and treatment. Overall, this work suggests that filamentous phage evolution can drive of eco-evolutionary feedbacks in bacterial populations, causing phenotypic and genetic changes that would not be anticipated from adaptation to the extrinsic environment alone.

The transgenerational inheritance of plant microbiota is fundamental to host fitness, however the ecological rules governing microbial assembly during the transition from flower to seed remain poorly understood. Therefore, we characterized the spatiotemporal dynamics of the soybean microbiota across developmental stages from vegetative to reproductive growth, and identified the specific seed-pod stages that drive a critical deterministic bottleneck for the recruitment of seed endophytes. Although the floral stage serves as a high-diversity recruitment keystone taxa dominated by stochastic processes, pod enclosure imposes rigorous host-mediated filtering and dispersal limitation, shifting the community toward a specialized "guardian" microbiota. By employing functional characterization and defined microbial community assays, we demonstrated that keystone taxa utilize niche partitioning and functional complementarity to provide collective resilience. The consortium may contribute to the reduction of salinity stress by stabilizing photosynthetic efficiency and suppresses Phytophthora sojae infection through synergizing direct antagonism with compensatory growth. Anatomical evidence suggests the soybean endocarp acts as a physical interface and ecological reservoir, facilitating the redistribution of maternal microbes into the maturing seed. Our findings define a precise "transmission window" for microbiota-based interventions, providing a roadmap for engineering more resilient crop-microbe associations across generations.

Microbial communities carry out important ecological functions. Their activities emerge from interactions between species, often potentiated by metabolic traits. We lack a quantitative understanding of how these traits shape community properties. Here, we present theory for microbial communities, leveraging concepts from quantitative microbial physiology. We focus on how steady-state metabolic exchanges between species determine their fractional abundances, given their biomass and byproduct yields on nutrients. We start by deriving formal conditions for the steady states of communities of microbes that grow, die, and cross-feed metabolites. We describe the metabolic stoichiometry of nutrient uptake and the formation of biomass and byproducts for each species in terms of charge- and chemical-element balanced reactions (macrochemical reactions). Byproducts function as nutrients for other species. Next, we express the relative abundances of species (living and dead), the net metabolic conversion of a community, and the biomass carrying capacity in terms of the metabolic stoichiometry, growth rates and death rates of the species. We show how niche creation can emerge from stoichiometric imbalances in cross-feeding communities. Finally, we discuss how relative species abundances depend on the Adenosine Triphosphate (ATP) stoichiometries of intracellular metabolism.

Dimethyl sulfide (DMS) is a central volatile sulfur intermediate in the global sulfur cycle, traditionally associated with marine ecosystems. However, despite significant advances, important gaps remain in our understanding of its metabolism in terrestrial environments. Here, we elucidate a complete DMS catabolic pathway for sulfur utilization in the soil bacterium Acinetobacter baylyi ADP1 using an integrative approach combining targeted metabolomics, genetic knockouts, and in vitro enzyme assays. The pathway consists of a series of oxidation reactions catalyzed by two-component monooxygenases, including newly identified enzymes responsible for the sequential conversion of DMS to dimethyl sulfoxide and then dimethyl sulfone. These steps are followed by previously reported downstream enzymes that form methanesulfinate and methanesulfonate, ultimately yielding sulfite for cysteine biosynthesis. Functional redundancy and substrate promiscuity characterize these monooxygenases, all of which are powered by a single flavin reductase. A genomic survey revealed that this pathway is widespread among plant-associated and soil-dwelling Proteobacteria, including Pseudomonas putida and Rhodococcus opacus, which were experimentally confirmed to grow on DMS. Our findings reveal a widespread terrestrial DMS metabolic route that may represent a significant, yet previously unrecognized, component of the global sulfur cycle.

From a "One Health" perspective, antibiotic resistance genes (ARGs) harbored by the plant microbiome pose a significant threat to public health, yet their ecological mechanisms under fungicide stress remain largely unexplored. Here, a comprehensive framework integrating selection, dispersal, antagonistic interactions, and horizontal gene transfer (HGT) is established to elucidate the ecological risks and assembly mechanisms of the tomato resistome under fungicide stress, using multi-omics and several validation experiments. The indirect/direct ecological risks of ARGs in aboveground tomato tissues increase by 1.69-93.81-fold and 1.29-123.49-fold under fungicide exposure, respectively, compared to the control. Dispersal and selection emerge as the dominant ecological processes shaping the resistome under fungicide stress, driven by antibiotic-resistant bacteria (ARB) with streamlined and multifunctional metabolic traits, respectively. A fluorescently labeled ARB migration model and an indigenous ARB-based conjugation model demonstrate that fungicides promote the upward dispersal of native ESKAPE pathogens and intensify HGT among them, facilitating the emergence of multidrug-resistant bacteria. Validation experiments confirm that fungicides induce metabolic reprogramming of flavonoid biosynthesis in roots, which enhances HGT by modulating various physiological phenotypes. These findings underscore the ecological risks posed by fungicides in promoting ARG dissemination within the plant microbiome through multiple ecological mechanisms.

Although horizontal gene transfer drives bacterial diversification, its contribution to chromosome-scale variation in human gut commensals remains unclear. This study demonstrated that human-associated bifidobacteria undergo extensive chromosomal transfer through natural transformation. Comparative genomics of coexisting Bifidobacterium pseudocatenulatum isolates from a single individual revealed extensive recombination signatures between the lineages. We experimentally reproduced this recombination by co-culturing strains, resulting in the transfer of multiple chromosomal regions and generation of mosaic genomes. Individual recombination tracts reached up to 247 kb per site, with cumulative replacements accounting for up to 28.9% of the recipient chromosome. These transfers occurred with heat-killed donors or purified DNA and were abolished by DNase, thereby identifying natural transformation as the underlying mechanism. Furthermore, we observed that environmental factors strongly influenced transformation frequency, suggesting that gut environmental conditions play a role regulating this process. Using natural transformation, we established a simple markerless genome-editing method that enables efficient gene deletions. Deletions of the Tad pili, ComEA-ComEC, or DprA-ComM-YraN gene clusters abolished transformation, defining the core machinery. The conservation of these genes across the genus Bifidobacterium and experimental demonstration of natural transformation in Bifidobacterium longum and Bifidobacterium breve indicate that natural transformation capacity is widespread within the genus. Our findings establish natural transformation as a key mechanism that promotes genome plasticity and contributes to adaptive evolution in bifidobacteria, thereby expanding our current understanding of horizontal gene transfer in the human gut microbiota.

Probiotics hold promise for enhancing coral resilience under climate-driven thermal stress, yet their mechanisms remain poorly understood. Although the bacterial genus Endozoicomonas has been proposed to benefit corals, in vivo evidence of beneficial effects on the host remains limited. Here, we establish Endozoicomonas acroporae Acr-14T as a coral probiotic and characterize its effects on the reef-building coral Stylophora pistillata. We show that E. acroporae Acr-14T enhances host thermal tolerance, colonizes coral tissues, and forms coral-associated microbial aggregates. Microbial profiling indicates that probiotic treatment is associated with reduced relative abundances of opportunistic microbes and enrichment of putatively beneficial taxa. To support transcriptomic analyses, we assembled a chromosome-level genome of S. pistillata clade 1 (Pacific lineage) and found that E. acroporae Acr-14T treatment mitigates heat-induced protein-folding stress and apoptotic signaling. Single-cell transcriptomics further revealed altered expression of genes involved in S-adenosylmethionine (SAMe) metabolism and pro-survival signaling in gastrodermal cells of probiotic-treated corals. Together, our results provide a cell-type-resolved view of host responses linked to Endozoicomonas-mediated coral thermal resilience and offer insight into molecular mechanisms implicated in host-microbe interactions under environmental stress.

The anaerobic oxidation of methane and C2+-alkanes is a dominant metabolism within hydrocarbon-rich deep-sea sediments and is largely mediated by alkane-oxidizing archaea in metabolic partnership with syntrophic sulfate-reducing bacteria. Although these processes fuel a diverse ecosystem, the viral component of alkane-rich sediments has historically been overlooked. We analyzed the viral assemblages in long-term sediment-free cultures of alkane-degrading organisms and found that abiotic factors such as incubation temperature had a greater correlation with community composition than with the phylogenetic patterns among individual viral species. No auxiliary metabolic genes (AMGs) directly involved in hydrocarbon oxidation or sulfate reduction were found, but the presence of candidate AMGs involved in heme synthesis pathways common in methane oxidizers hints at a possible viral impact on alkane degradation. We also examined potential host-virus pairs using CRISPR- and tRNA-based methods. Lastly, we identified the presence of nosD-like proteins in viruses from sediment-derived systems that are not present in water column datasets; their distribution, genomic context, and lack of canonical nosD characteristics suggest an alternate adhesion-related role in sediment communities. The number of new viruses obtained from these multi-year enrichment cultures and their potential roles in mediating host physiology illustrate the importance of studying the viral component in laboratory and environmental systems.

Ferdinand Cohn observed abundant filamentous bacteria in drinking water wells in 1870 that he named Crenothrix polyspora. Subsequent research has revealed the methanotrophic metabolism of Crenothrix bacteria and their disproportionately high activity in stratified lakes compared to unicellular methanotrophs, yet laboratory cultivation has proven elusive, leaving the ecophysiology of Crenothrix bacteria largely unknown. Here we report the isolation of two methanotrophic strains of the "lacustrine Crenothrix" clade from an iron-rich wetland and reveal their unique cell biology and ecology. We demonstrate that the strains are microaerobic and grow as filaments of cells, which are connected by unidirectionally oriented structures. The strains have broad genomic repertoires for addressing O2 limitation that are uniquely associated with lacustrine Crenothrix compared to related clades based on genome data. Aligning with laboratory observations, we identify lacustrine Crenothrix bacteria along potential redox gradients in the wetland at iron-rich snow sites, and we also detect such bacteria in diverse global ecosystems based on public metagenome searches. Together, our data strongly point to an ecophysiology of lacustrine Crenothrix bacteria that is tightly linked to O2 limitation, and we propose that the strains uniquely store or share metabolic intermediates between cells in filaments to thrive under such conditions. Our cultivation-based findings for these strains, which we name Allocrenothrix methanica, provide new insights into the diversity, evolution, and ecology of filamentous methanotrophs, connecting over 150 years of microbiology research and opening vast new opportunities to investigate bacteria contributing to the global methane cycle under O2 limitation.