ISME communications最新文献

Unicellular green picophytoplankton from the Mamiellales order are pervasive in marine ecosystems and susceptible to infections by prasinoviruses, large double-stranded DNA viruses within the Nucleocytoviricota phylum. We developed a double-stranded DNA virus enrichment and shotgun sequencing method, and successfully assembled 80 prasinovirus genomes from 43 samples in the South China Sea. Our research delivered the first direct estimation of 94% accuracy in correlating genome similarity to host range. Stirkingly, our analyses uncovered unexpected host-switching across diverse algal lineages, challenging the existing paradigms of host-virus co-speciation and revealing the dynamic nature of viral evolution. We also detected six instances of horizontal gene transfer between prasinoviruses and their hosts, including a novel alternative oxidase. Additionally, diversifying selection on a major capsid protein suggests an ongoing co-evolutionary arms race. These insights not only expand our understanding of prasinovirus genomic diversity but also highlight the intricate evolutionary mechanisms driving their ecological success and shaping broader virus-host interactions in marine environments.

Bacteriophages (phages) are increasingly considered for both treatment and early detection of bacterial pathogens given their specificity and rapid infection kinetics. Here, we exploit an engineered phage expressing nanoluciferase to detect signals associated with Pseudomonas aeruginosa lysis spanning single cells to populations. Using several P. aeruginosa strains we found that the latent period, burst size, fraction of infected cells, and efficiency of plating inferred from fluorescent light intensity signals were consistent with inferences from conventional population assays. Notably, imaging-based traits were obtained in minutes to hours in contrast to the use of overnight plaques, which opens the possibility to study infection dynamics in spatial and/or temporal contexts where plaque development is infeasible. These findings support the use of engineered phages to study infection kinetics of virus-cell interactions in complex environments and potentially accelerate the determination of viral host range in therapeutically relevant contexts.

Microbes play a crucial role in the arsenic biogeochemical cycle through specific metabolic pathways to adapt to arsenic toxicity. However, the different arsenic-detoxification strategies between prokaryotic and eukaryotic microbes are poorly understood. This hampers our comprehension of how microbe-arsenic interactions drive the arsenic cycle and the development of microbial methods for remediation. In this study, we utilized conserved protein domains from 16 arsenic biotransformation genes (ABGs) to search for homologous proteins in 670 microbial genomes. Prokaryotes exhibited a wider species distribution of arsenic reduction- and arsenic efflux-related genes than fungi, whereas arsenic oxidation-related genes were more prevalent in fungi than in prokaryotes. This was supported by significantly higher acr3 (arsenite efflux permease) expression in bacteria (upregulated 3.72-fold) than in fungi (upregulated 1.54-fold) and higher aoxA (arsenite oxidase) expression in fungi (upregulated 5.11-fold) than in bacteria (upregulated 2.05-fold) under arsenite stress. The average values of nonsynonymous substitutions per nonsynonymous site to synonymous substitutions per synonymous site (dN/dS) of homologous ABGs were higher in archaea (0.098) and bacteria (0.124) than in fungi (0.051). Significant negative correlations between the dN/dS of ABGs and species distribution breadth and gene expression levels in archaea, bacteria, and fungi indicated that microbes establish the distinct strength of purifying selection for homologous ABGs. These differences contribute to the distinct arsenic metabolism pathways in prokaryotic and eukaryotic microbes. These observations facilitate a significant shift from studying individual or several ABGs to characterizing the comprehensive microbial strategies of arsenic detoxification.

Leaf-associated microbial communities can promote plant health and resistance to biotic and abiotic stresses. However, the importance of environmental cues in the assembly of the leaf endo- and epi-microbiota remains elusive. Here, we aimed to investigate the impact of seasonal environmental variations, on the establishment of the leaf microbiome, focusing on long-term changes (five years) in bacterial, fungal, and nonfungal eukaryotic communities colonizing the surface and endosphere of six wild Arabidopsis thaliana populations. While leaf-microbial communities were found to be highly stochastic, the leaf niche had a predominant importance with endophytic microbial communities consistently exhibiting a lower diversity and variability. Among environmental factors, radiation- and humidity-related factors are the most important drivers of diversity patterns in the leaf, with stronger effects on epiphytic communities. Using linear models, we identified 30 important genera whose relative abundance in leaf compartments could be modeled from environmental variables, suggesting specific niche preferences for these taxa. With the hypothesis that environmental factors could impact interactions within microbial communities, we analyzed the seasonal patterns of microbial interaction networks across leaf compartments. We showed that epiphytic networks are more complex than endophytic and that the complexity and connectivity of these networks are partially correlated with the mentioned environmental cues. Our results indicate that humidity and solar radiation function as major environmental cues shaping the phyllosphere microbiome at both micro (leaf compartment) and macro (site) scales. These findings could have practical implications for predicting and developing field-adapted microbes in the face of global change.

Controlled greenhouse studies have shown the numerous ways that soil microbes can impact plant growth and development. However, natural soil communities are highly complex, and plants interact with many bacterial and fungal taxa simultaneously. Due to logistical challenges associated with manipulating more complex microbiome communities, how microbial communities impact emergent patterns of plant growth therefore remains poorly understood. For instance, do the interactions between bacteria and fungi generally yield additive (i.e. sum of their parts) or nonadditive, higher order plant growth responses? Without this information, our ability to accurately predict plant responses to microbial inoculants is weakened. To address these issues, we conducted a meta-analysis to determine the type (additive or higher-order, nonadditive interactions), frequency, direction (positive or negative), and strength that bacteria and mycorrhizal fungi (arbuscular and ectomycorrhizal) have on six phenotypic plant growth responses. Our results demonstrate that co-inoculations of bacteria and mycorrhizal fungi tend to have positive additive effects on many commonly reported plant responses. However, ectomycorrhizal plant shoot height responds positively and nonadditively to co-inoculations of bacteria and ectomycorrhizal fungi, and the strength of additive effects also differs between mycorrhizae type. These findings suggest that inferences from greenhouse studies likely scale to more complex field settings and that inoculating plants with diverse, beneficial microbes is a sound strategy to support plant growth.

Diverse populations of bacteriophages infect and coevolve with their bacterial hosts. Although host recognition and infection occur within microbiomes, the molecular mechanisms underlying host-phage interactions within a community context remain poorly studied. The biofilms (rinds) of aged cheeses contain taxonomically diverse microbial communities that follow reproducible growth patterns and can be manipulated under laboratory conditions. In this study, we use cheese as a model for studying phage-microbe interactions by identifying and characterizing a tractable host-phage pair co-occurring within a model Brie-like community. We isolated a novel bacteriophage, TS33, that kills Hafnia sp. JB232, a member of the model community. TS33 is easily propagated in the lab and naturally co-occurs in the cheese community, rendering it a prime candidate for the study of host-phage interactions. We performed growth assays of the Hafnia, TS33, and the fungal community members, Geotrichum candidum and Penicillium camemberti. Employing Random Barcode Transposon Sequencing experiments, we identified candidate host factors that contribute to TS33 infectivity, many of which are homologs of bacterial O-antigen genes. Hafnia mutants in these genes exhibit decreased susceptibility to phage infection, but experience negative fitness effects in the presence of the fungi. Therefore, mutations in O-antigen biosynthesis homologs may have antagonistic pleiotropic effects in Hafnia that have major consequences for its interactions with the rest of the community. Ongoing and future studies aim to unearth the molecular mechanisms by which the O-antigen of Hafnia mediates its interactions with its viral and fungal partners.

The gut microbiota of the marine herbivorous fish Kyphosus sydneyanus are thought to play an important role in host nutrition by supplying short-chain fatty acids (SCFAs) through fermentation of dietary red and brown macroalgae. Here, using 645 metagenome-assembled genomes (MAGs) from wild fish, we determined the capacity of different bacterial taxa to degrade seaweed carbohydrates along the gut. Most bacteria (99%) were unclassified at the species level. Gut communities and CAZyme-related transcriptional activity were dominated by Bacteroidia and Clostridia. Both classes possess genes CAZymes acting on internal polysaccharide bonds, suggesting their role initiating glycan depolymerization, followed by rarer Gammaproteobacteria and Verrucomicrobiae. Results indicate that Bacteroidia utilize substrates in both brown and red algae, whereas other taxa, namely, Clostridia, Bacilli, and Verrucomicrobiae, utilize mainly brown algae. Bacteroidia had the highest CAZyme gene densities overall, and Alistipes were especially enriched in CAZyme gene clusters (n = 73 versus just 62 distributed across all other taxa), pointing to an enhanced capacity for macroalgal polysaccharide utilization (e.g., alginate, laminarin, and sulfated polysaccharides). Pairwise correlations of MAG relative abundances and encoded CAZyme compositions provide evidence of potential inter-species collaborations. Co-abundant MAGs exhibited complementary degradative capacities for specific substrates, and flexibility in their capacity to source carbon (e.g., glucose- or galactose-rich glycans), possibly facilitating coexistence via niche partitioning. Results indicate the potential for collaborative microbial carbohydrate metabolism in the K. sydneyanus gut, that a greater variety of taxa contribute to the breakdown of brown versus red dietary algae, and that Bacteroidia encompass specialized macroalgae degraders.

Electrogenic biofilms, which have attracted considerable attention in simultaneous wastewater treatment and energy recovery in bioelectrochemical systems, are regulated by chemical communication and potassium channel-mediated electrical signaling. However, how these two communication pathways interact with each other has not been thoroughly investigated. This study first explored the roles of chemical communication, including intracellular bis-(3'-5')-cyclic dimeric guanosine monophosphate (c-di-GMP) and extracellular N-acyl-homoserine lactone (AHL)-mediated quorum sensing, in electrogenic biofilm formation through an integrated analysis of transcriptomics and metabolomics. Electrical signaling disruption inhibited the formation and electroactivity of Geobacter sulfurreducens biofilm, which was mainly ascribed to the reduction in biofilm viability and extracellular protein/polysaccharide ratio. The upregulation of expression levels of genes encoding c-di-GMP and AHL synthesis by transcriptomic analysis, and the increased secretion of N-butanoyl-L-homoserine lactone by metabolomic analysis confirmed the enhancement of chemical communication under electrical signaling disruption, thus indicating a compensatory mechanism among different signaling pathways. Furthermore, protein-protein interaction network showed the convergence of different signaling pathways, with c-di-GMP-related genes acting as central bridges. This study highlights the interaction of different signaling pathways, especially the resilience of c-di-GMP signaling to adverse external stresses, thereby laying the foundation for facilitating electrogenic biofilm formation under adverse conditions in practical applications.

Anaerobic protists frequently harbour methanogenic archaea, which apparently contribute to the hosts' fermentative metabolism by consuming excess H₂. However, the ecological properties of endosymbiotic methanogens remain elusive in many cases. Here we investigated the ecology and genome of the endosymbiotic methanogen of the Cononympha protists in the hindgut of the termite Coptotermes formosanus. Microscopic and 16S rRNA amplicon sequencing analyses revealed that a single species, designated here "Candidatus Methanobrevibacter cononymphae", is associated with both Cononympha leidyi and Cononympha koidzumii and that its infection rate in Cononympha cells varied from 0.0% to 99.8% among termite colonies. Fine-scale network analysis indicated that multiple 16S rRNA sequence variants coexisted within a single host cell and that identical variants were present in both Cononympha species and also on the gut wall. Thus, "Ca. Methanobrevibacter cononymphae" is a facultative endosymbiont, transmitted vertically with frequent exchanges with the gut environment. Indeed, transmission electron microscopy showed escape or uptake of methanogens from/by a Cononympha cell. The genome of "Ca. Methanobrevibacter cononymphae" showed features consistent with its facultative lifestyle: i.e., the genome size (2.7 Mbp) comparable to those of free-living relatives; the pseudogenization of the formate dehydrogenase gene fdhA, unnecessary within the non-formate-producing host cell; the dependence on abundant acetate in the host cell as an essential carbon source; and the presence of a catalase gene, required for colonization on the microoxic gut wall. Our study revealed a versatile endosymbiosis between the methanogen and protists, which may be a strategy responding to changing conditions in the termite gut.

While the air microbiome and its diversity are essential for human health and ecosystem resilience, comprehensive air microbial diversity monitoring has remained rare, so that little is known about the air microbiome's composition, distribution, or functionality. Here we show that nanopore sequencing-based metagenomics can robustly assess the air microbiome in combination with active air sampling through liquid impingement and tailored computational analysis. We provide fast and portable laboratory and computational approaches for air microbiome profiling, which we leverage to robustly assess the taxonomic composition of the core air microbiome of a controlled greenhouse environment and of a natural outdoor environment. We show that long-read sequencing can resolve species-level annotations and specific ecosystem functions through de novo metagenomic assemblies despite the low amount of fragmented DNA used as an input for nanopore sequencing. We then apply our pipeline to assess the diversity and variability of an urban air microbiome, using Barcelona, Spain, as an example; this randomized experiment gives first insights into the presence of highly stable location-specific air microbiomes within the city's boundaries, and showcases the robust microbial assessments that can be achieved through automatable, fast, and portable nanopore sequencing technology.