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Streptomyces bacteria are known for their prolific production of secondary metabolites, many of which have been widely used in human medicine, agriculture and animal health. To guide the effective prioritization of specific biosynthetic gene clusters (BGCs) for drug development and targeting the most prolific producer strains, knowledge about phylogenetic relationships of Streptomyces species, genome-wide diversity and distribution patterns of BGCs is critical. We used genomic and phylogenetic methods to elucidate the diversity of major classes of BGCs in 1,110 publicly available Streptomyces genomes. Genome mining of Streptomyces reveals high diversity of BGCs and variable distribution patterns in the Streptomyces phylogeny, even among very closely related strains. The most common BGCs are non-ribosomal peptide synthetases, type 1 polyketide synthases, terpenes, and lantipeptides. We also found that numerous Streptomyces species harbor BGCs known to encode antitumor compounds. We observed that strains that are considered the same species can vary tremendously in the BGCs they carry, suggesting that strain-level genome sequencing can uncover high levels of BGC diversity and potentially useful derivatives of any one compound. These findings suggest that a strain-level strategy for exploring secondary metabolites for clinical use provides an alternative or complementary approach to discovering novel pharmaceutical compounds from microbes.

Prokaryotic evolution is affected by horizontal transfer of genetic material through recombination. Inference of an evolutionary tree of bacteria thus relies on accurate identification of the population genetic structure and recombination-derived mosaicism. Rapidly growing databases represent a challenge for computational methods to detect recombinations in bacterial genomes. We introduce a novel algorithm called fastGEAR which identifies lineages in diverse microbial alignments, and recombinations between them and from external origins. The algorithm detects both recent recombinations (affecting a few isolates) and ancestral recombinations between detected lineages (affecting entire lineages), thus providing insight into recombinations affecting deep branches of the phylogenetic tree. In simulations, fastGEAR had comparable power to detect recent recombinations and outstanding power to detect the ancestral ones, compared with state-of-the-art methods, often with a fraction of computational cost. We demonstrate the utility of the method by analyzing a collection of 616 whole-genomes of a recombinogenic pathogen Streptococcus pneumoniae, for which the method provided a high-resolution view of recombination across the genome. We examined in detail the penicillin-binding genes across the Streptococcus genus, demonstrating previously undetected genetic exchanges between different species at these three loci. Hence, fastGEAR can be readily applied to investigate mosaicism in bacterial genes across multiple species. Finally, fastGEAR correctly identified many known recombination hotspots and pointed to potential new ones. Matlab code and Linux/Windows executables are available at https://users.ics.aalto.fi/~pemartti/fastGEAR/ (last accessed February 6, 2017).

Streptococcus consists of ecologically diverse species, some of which are important pathogens of humans and animals. We sought to quantify and compare the frequencies and characteristics of within-species recombination in the pan-genomes of Streptococcus agalactiae, Streptococcus pyogenes and Streptococcus suis . We used 1081, 1813 and 1204 publicly available genome sequences of each species, respectively. Based on their core genomes, S. agalactiae had the highest relative rate of recombination to mutation (11.5743) compared to S. pyogenes (1.03) and S. suis (0.57). The proportion of the species pan-genome that have had a history of recombination was 12.85%, 24.18% and 20.50% of the pan-genomes of each species, respectively. The composition of recombining genes varied among the three species, and some of the most frequently recombining genes are implicated in adhesion, colonization, oxidative stress response and biofilm formation. For each species, a total of 22.75%, 29.28% and 18.75% of the recombining genes were associated with prophages. The cargo genes of integrative conjugative elements and integrative and mobilizable elements contained genes associated with antimicrobial resistance and virulence. Homologous recombination and mobilizable pan-genomes enable the creation of novel combinations of genes and sequence variants, and the potential for high-risk clones to emerge.

The emergence of methicillin-resistant Staphylococcus aureus (MRSA) poses an important threat in human and animal health. In this study, we ask whether resistance and virulence genes in S. aureus are homogeneously distributed or constrained by different animal hosts. We carried out whole genome sequencing of 114 S. aureus isolates from ten species of animals sampled from four New England states (USA) in 2017–2019. The majority of the isolates came from cats, cows and dogs. The maximum likelihood phylogenetic tree based on the alignment of 89,143 single nucleotide polymorphisms of 1173 core genes reveal 31 sequence types (STs). The most common STs were ST5, ST8, ST30, ST133 and ST2187. Every genome carried at least eight acquired resistance genes. Genes related to resistance found in all genomes included norA (fluoroquinolone) , arlRS (fluoroquinolone) , lmrS (multidrug) , tet(38) (tetracycline) and mepAR (multidrug and tigecycline resistance). The most common superantigen genes were tsst-1 , sea and sec . Acquired antibiotic resistance ( n  = 10) and superantigen ( n  = 9) genes of S. aureus were widely shared between S. aureus lineages and between strains from different animal hosts. These analyses provide insights for considering bacterial gene sharing when developing strategies to combat the emergence of high-risk clones in animals.

Bloodstream infections caused by the opportunistic pathogen Klebsiella pneumoniae are associated with adverse health complications and high mortality rates. Antimicrobial resistance (AMR) limits available treatment options, thus exacerbating its public health and clinical burden. Here, we aim to elucidate the population structure of K. pneumoniae in bloodstream infections from a single medical center and the drivers that facilitate the dissemination of AMR. Analysis of 136 short-read genome sequences complemented with 12 long-read sequences shows the population consisting of 94 sequence types (STs) and 99 clonal groups, including globally distributed multidrug resistant and hypervirulent clones. In vitro antimicrobial susceptibility testing and in silico identification of AMR determinants reveal high concordance (90.44–100%) for aminoglycosides, beta-lactams, carbapenems, cephalosporins, quinolones, and sulfonamides. IncF plasmids mediate the clonal (within the same lineage) and horizontal (between lineages) transmission of the extended-spectrum beta-lactamase gene bla CTX-M-15 . Nearly identical plasmids are recovered from isolates over a span of two years indicating long-term persistence. The genetic determinants for hypervirulence are carried on plasmids exhibiting genomic rearrangement, loss, and/or truncation. Our findings highlight the importance of considering both the genetic background of host strains and the routes of plasmid transmission in understanding the spread of AMR in bloodstream infections. Authors perform a genomic analyses of 136 Klebsiella pneumoniae isolates, revealing that both the genetic background of host strains and the routes of plasmid transmission influence the spread of antimicrobial resistance in bloodstream infections.

Microbes in marine sediments constitute a large percentage of the global marine ecosystem and function to maintain a healthy food web. In continental shelf habitats such as the Gulf of Maine (GoM), relatively little is known of the microbial community abundance, biodiversity, and natural product potential. This report is the first to provide a time-series assessment (2017–2020) of the sediment microbial structure in areas open and closed to fishing within the Stellwagen Bank National Marine Sanctuary (SBNMS). A whole metagenome sequencing (WMS) approach was used to characterize the sediment microbial community. Taxonomic abundance was calculated across seven geographic sites with 14 individual sediment samples collected during the summer and fall seasons. Bioinformatics analyses identified more than 5900 different species across multiple years. Non-metric multidimensional scaling methods and generalized linear models demonstrated that species richness was inversely associated with fishing exposure levels and varied by year. Additionally, the discovery of 12 unique biosynthetic gene clusters (BGCs) collected across sites confirmed the potential for medically relevant natural product discovery in the SBNMS. This study provides a practical assessment of how fishing exposure and temporal trends may affect microbial community structure in a coastal marine sanctuary.

Background The opportunistic bacterium Escherichia coli can invade normally sterile sites in the human body, potentially leading to life-threatening organ dysfunction and even death. However, our understanding of the evolutionary processes that shape its genetic diversity in this sterile environment remains limited. Here, we aim to quantify the frequency and characteristics of homologous recombination in E. coli from bloodstream infections. Results Analysis of 557 short-read genome sequences revealed that the propensity to exchange DNA by homologous recombination varies within a distinct population (bloodstream) at narrow geographic (Dartmouth Hitchcock Medical Center, New Hampshire, USA) and temporal (years 2016 – 2022) scope. We identified the four largest monophyletic sequence clusters in the core genome phylogeny that are represented by prominent sequence types (ST): BAPS1 (mainly ST95), BAPS4 (mainly ST73), BAPS10 (mainly ST131), BAPS14 (mainly ST58). We show that the four dominant clusters vary in different characteristics of recombination: number of single nucleotide polymorphisms due to recombination, number of recombination blocks, cumulative bases in recombination blocks, ratio of probabilities that a given site was altered through recombination and mutation (r/m), and ratio of rates at which recombination and mutation occurred (ρ/θ). Each sequence cluster contains a unique set of antimicrobial resistance (AMR) and virulence genes that have experienced recombination. Common among the four sequence clusters were the recombined virulence genes with functions associated with the Curli secretion channel ( csgG ) and ferric enterobactin transport ( entEF , fepEG ). We did not identify any one recombined AMR gene that was present in all four sequence clusters. However, AMR genes mdtABC , baeSR, emrKY and tolC had experienced recombination in sequence clusters BAPS4, BAPS10, and BAPS14. These differences lie in part on the contributions of vertically inherited ancestral recombination and contemporary branch-specific recombination, with some genomes having relatively higher proportions of recombined DNA. Conclusions Our results highlight the variation in the propensity to exchange DNA via homologous recombination within a distinct population at narrow geographic and temporal ranges. Understanding the sources of the genetic variation in invasive E. coli will help inform the implementation of effective strategies to reduce the burden of disease and AMR.

We show that Streptomyces biogeography in soils across North America is influenced by the regional diversification of microorganisms due to dispersal limitation and genetic drift. Streptomyces spp. form desiccation-resistant spores, which can be dispersed on the wind, allowing for a strong test of whether dispersal limitation governs patterns of terrestrial microbial diversity. We employed an approach that has high sensitivity for determining the effects of genetic drift. Specifically, we examined the genetic diversity and phylogeography of physiologically similar Streptomyces strains isolated from geographically distributed yet ecologically similar habitats. We found that Streptomyces beta diversity scales with geographic distance and both beta diversity and phylogenetic diversity manifest in a latitudinal diversity gradient. This pattern of Streptomyces biogeography resembles patterns seen for diverse species of plants and animals, and we therefore evaluated these data in the context of ecological and evolutionary hypotheses proposed to explain latitudinal diversity gradients. The data are consistent with the hypothesis that niche conservatism limits dispersal, and historical patterns of glaciation have limited the time for speciation in higher-latitude sites. Most notably, higher-latitude sites have lower phylogenetic diversity, higher phylogenetic clustering, and evidence of range expansion from lower latitudes. In addition, patterns of beta diversity partition with respect to the glacial history of sites. Hence, the data support the hypothesis that extant patterns of Streptomyces biogeography have been driven by historical patterns of glaciation and are the result of demographic range expansion, dispersal limitation, and regional diversification due to drift. IMPORTANCE Biogeographic patterns provide insight into the evolutionary and ecological processes that govern biodiversity. However, the evolutionary and ecological processes that govern terrestrial microbial diversity remain poorly characterized. We evaluated the biogeography of the genus Streptomyces to show that the diversity of terrestrial bacteria is governed by many of the same processes that govern the diversity of many plant and animal species. While bacteria of the genus Streptomyces are a preeminent source of antibiotics, their evolutionary history, biogeography, and biodiversity remain poorly characterized. The observations we describe provide insight into the drivers of Streptomyces biodiversity and the processes that underlie microbial diversification in terrestrial habitats. Biogeographic patterns provide insight into the evolutionary and ecological processes that govern biodiversity. However, the evolutionary and ecological processes that govern terrestrial microbial diversity remain poorly characterized. We evaluated the biogeography of the genus Streptomyces to show that the diversity of terrestrial bacteria is governed by many of the same processes that govern the diversity of many plant and animal species. While bacteria of the genus Streptomyces are a preeminent source of antibiotics, their evolutionary history, biogeography, and biodiversity remain poorly characterized. The observations we describe provide insight into the drivers of Streptomyces biodiversity and the processes that underlie microbial diversification in terrestrial habitats.

Listeria monocytogenes (Lm) is an opportunistic foodborne pathogen responsible for gastrointestinal illnesses and life-threatening invasive infections. Antimicrobial resistance, virulence, and rapid adaptation to stressful environments in Lm lie in part on its mobile genetic elements (MGE). Here, we aim to characterize the MGE pool of a clinical Lm population using 936 genomes sampled across New York State (USA) from 2000 – 2021. We built a network based on sequence homology among putative MGEs. Within the network are communities of densely interconnected MGEs indicating high genetic similarity in their DNA regions. Although most connections involve the same MGE type, subsets within the network link different MGE types (plasmid-transposon, phage-plasmid). Phages and transposons did not share any genetic connections, suggesting impermeable barriers of exchange between them. Genes involved in stress tolerance are overrepresented in plasmids and transposons, and are mobile between vehicles. Analysis of long-read sequences of a subset of our dataset ( n  = 37) and publicly available, globally distributed complete genomes ( n  = 425) recapitulated the MGE connections we observed. Our findings reveal a structured but interconnected network of genetic exchanges between different mobile DNA vehicles. Genetic exchanges between MGEs shape Lm intra-species variation, adaptive potential, and rapid dissemination of clinically relevant traits at short timescales. This study shows that the mobile genetic elements of Listeria monocytogenes exhibit a structured but interconnected network of genetic exchanges. The authors found dense interconnections of similar sequences among phages, plasmids and transposons.

Background Cronobacter sakazakii is an emerging opportunistic bacterial pathogen known to cause neonatal and pediatric infections, including meningitis, necrotizing enterocolitis, and bacteremia. Multiple disease outbreaks of C. sakazakii have been documented in the past few decades, yet little is known of its genomic diversity, adaptation, and evolution. Here, we analyzed the pan-genome characteristics and phylogenetic relationships of 237 genomes of C. sakazakii and 48 genomes of related Cronobacter species isolated from diverse sources. Results The C. sakazakii pan-genome contains 17,158 orthologous gene clusters, and approximately 19.5% of these constitute the core genome. Phylogenetic analyses reveal the presence of at least ten deep branching monophyletic lineages indicative of ancestral diversification. We detected enrichment of functions involved in proton transport and rotational mechanism in accessory genes exclusively found in human-derived strains. In environment-exclusive accessory genes, we detected enrichment for those involved in tryptophan biosynthesis and indole metabolism. However, we did not find significantly enriched gene functions for those genes exclusively found in food strains. The most frequently detected virulence genes are those that encode proteins associated with chemotaxis, enterobactin synthesis, ferrienterobactin transporter, type VI secretion system, galactose metabolism, and mannose metabolism. The genes fos which encodes resistance against fosfomycin, a broad-spectrum cell wall synthesis inhibitor, and mdf(A) which encodes a multidrug efflux transporter were found in nearly all genomes. We found that a total of 2991 genes in the pan-genome have had a history of recombination. Many of the most frequently recombined genes are associated with nutrient acquisition, metabolism and toxin production. Conclusions Overall, our results indicate that the presence of a large accessory gene pool, ability to switch between ecological niches, a diverse suite of antibiotic resistance, virulence and niche-specific genes, and frequent recombination partly explain the remarkable adaptability of C. sakazakii within and outside the human host. These findings provide critical insights that can help define the development of effective disease surveillance and control strategies for Cronobacter -related diseases.