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1. The roles of antimicrobial resistance, phage diversity, isolation source and selection in shaping the genomic architecture of Bacillus anthracis

   https://doi.org/10.1099/mgen.0.000616  

   Bruce, Spencer A.; Huang, Yen-Hua; Kamath, Pauline L.; van Heerden, Henriette; Turner, Wendy C. (August 2021, Microbial Genomics)

   null (Ed.)

   Bacillus anthracis, the causative agent of anthrax disease, is a worldwide threat to livestock, wildlife and public health. While analyses of genetic data from across the globe have increased our understanding of this bacterium’s population genomic structure, the influence of selective pressures on this successful pathogen is not well understood. In this study, we investigate the effects of antimicrobial resistance, phage diversity, geography and isolation source in shaping population genomic structure. We also identify a suite of candidate genes potentially under selection, driving patterns of diversity across 356 globally extant B. anthracis genomes. We report ten antimicrobial resistance genes and 11 different prophage sequences, resulting in the first large-scale documentation of these genetic anomalies for this pathogen. Results of random forest classification suggest genomic structure may be driven by a combination of antimicrobial resistance, geography and isolation source, specific to the population cluster examined. We found strong evidence that a recombination event linked to a gene involved in protein synthesis may be responsible for phenotypic differences between comparatively disparate populations. We also offer a list of genes for further examination of B. anthracis evolution, based on high-impact single nucleotide polymorphisms (SNPs) and clustered mutations. The information presented here sheds new light on the factors driving genomic structure in this notorious pathogen and may act as a road map for future studies aimed at understanding functional differences in terms of B. anthracis biogeography, virulence and evolution. 

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2. Contrasting continental patterns of adaptive population divergence in the holarctic ectomycorrhizal fungus Boletus edulis

   https://doi.org/10.1111/nph.18521  

   Tremble, Keaton; Hoffman, J. I.; Dentinger, Bryn T. (January 2023, New Phytologist)

   Summary In the hyperdiverse fungi, the process of speciation is virtually unknown, including for the > 20 000 species of ectomycorrhizal mutualists. To understand this process, we investigated patterns of genome‐wide differentiation in the ectomycorrhizal porcini mushroom, Boletus edulis , a globally distributed species complex with broad ecological amplitude. By whole‐genome sequencing 160 individuals from across the Northern Hemisphere, we genotyped 792 923 single nucleotide polymorphisms to characterize patterns of genome‐wide differentiation and to identify the adaptive processes shaping global population structure. We show that B. edulis exhibits contrasting patterns of genomic divergence between continents, with multiple lineages present across North America, while a single lineage dominates Europe. These geographical lineages are inferred to have diverged 1.62–2.66 million years ago, during a period of climatic upheaval and the onset of glaciation in the Pliocene–Pleistocene boundary. High levels of genomic differentiation were observed among lineages despite evidence of substantial and ongoing introgression. Genome scans, demographic inference, and ecological niche models suggest that genomic differentiation is maintained by environmental adaptation, not physical isolation. Our study uncovers striking patterns of genome‐wide differentiation on a global scale and emphasizes the importance of local adaptation and ecologically mediated divergence, rather than prezygotic barriers such as allopatry or genomic incompatibility, in fungal population differentiation. 

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3. Phylogenomics reveals extensive misidentification of fungal strains from the genus Aspergillus

   https://doi.org/10.1128/spectrum.03980-23  

   Steenwyk, Jacob L; Balamurugan, Charu; Raja, Huzefa A; Gonçalves, Carla; Li, Ningxiao; Martin, Frank; Berman, Judith; Oberlies, Nicholas H; Gibbons, John G; Goldman, Gustavo H; et al (April 2024, Microbiology Spectrum)

   Alanio, Alexandre (Ed.)

   ABSTRACT Modern taxonomic classification is often based on phylogenetic analyses of a few molecular markers, although single-gene studies are still common. Here, we leverage genome-scale molecular phylogenetics (phylogenomics) of species and populations to reconstruct evolutionary relationships in a dense data set of 710 fungal genomes from the biomedically and technologically important genusAspergillus. To do so, we generated a novel set of 1,362 high-quality molecular markers specific forAspergillusand provided profile Hidden Markov Models for each, facilitating their use by others. Examining the resulting phylogeny helped resolve ongoing taxonomic controversies, identified new ones, and revealed extensive strain misidentification (7.59% of strains were previously misidentified), underscoring the importance of population-level sampling in species classification. These findings were corroborated using the current standard, taxonomically informative loci. These findings suggest that phylogenomics of species and populations can facilitate accurate taxonomic classifications and reconstructions of the Tree of Life.IMPORTANCEIdentification of fungal species relies on the use of molecular markers. Advances in genomic technologies have made it possible to sequence the genome of any fungal strain, making it possible to use genomic data for the accurate assignment of strains to fungal species (and for the discovery of new ones). We examined the usefulness and current limitations of genomic data using a large data set of 710 publicly available genomes from multiple strains and species of the biomedically, agriculturally, and industrially important genusAspergillus. Our evolutionary genomic analyses revealed that nearly 8% of publicly availableAspergillusgenomes are misidentified. Our work highlights the usefulness of genomic data for fungal systematic biology and suggests that systematic genome sequencing of multiple strains, including reference strains (e.g., type strains), of fungal species will be required to reduce misidentification errors in public databases. 

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4. Whole genome analyses reveal weak signatures of population structure and environmentally associated local adaptation in an important North American pollinator, the bumble bee Bombus vosnesenskii

   https://doi.org/10.1111/mec.17125  

   Heraghty, Sam D.; Jackson, Jason M.; Lozier, Jeffrey D. (September 2023, Molecular Ecology)

   Abstract Studies of species that experience environmental heterogeneity across their distributions have become an important tool for understanding mechanisms of adaptation and predicting responses to climate change. We examine population structure, demographic history and environmentally associated genomic variation inBombus vosnesenskii, a common bumble bee in the western USA, using whole genome resequencing of populations distributed across a broad range of latitudes and elevations. We find thatB. vosnesenskiiexhibits minimal population structure and weak isolation by distance, confirming results from previous studies using other molecular marker types. Similarly, demographic analyses with Sequentially Markovian Coalescent models suggest that minimal population structure may have persisted since the last interglacial period, with genomes from different parts of the species range showing similar historical effective population size trajectories and relatively small fluctuations through time. Redundancy analysis revealed a small amount of genomic variation explained by bioclimatic variables. Environmental association analysis with latent factor mixed modelling (LFMM2) identified few outlier loci that were sparsely distributed throughout the genome and although a few putative signatures of selective sweeps were identified, none encompassed particularly large numbers of loci. Some outlier loci were in genes with known regulatory relationships, suggesting the possibility of weak selection, although compared with other species examined with similar approaches, evidence for extensive local adaptation signatures in the genome was relatively weak. Overall, results indicateB. vosnesenskiiis an example of a generalist with a high degree of flexibility in its environmental requirements that may ultimately benefit the species under periods of climate change. 

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5. Comparing microbiological and molecular diagnostic tools for the surveillance of anthrax

   https://doi.org/10.1371/journal.pntd.0012122  

   Ochai, Sunday Ochonu; Hassim, Ayesha; Dekker, Edgar H; Magome, Thuto; Lekota, Kgaugelo Edward; Makgabo, S Marcus; de_Klerk-Loris, Lin-Mari; van_Schalkwyk, Louis O; Kamath, Pauline L; Turner, Wendy C; et al (November 2024, PLOS Neglected Tropical Diseases)

   Chang, Yung-Fu (Ed.)

   The diagnosis of anthrax, a zoonotic disease caused byBacillus anthraciscan be complicated by detection of closely related species. Conventional diagnosis of anthrax involves microscopy, culture identification of bacterial colonies and molecular detection. Genetic markers used are often virulence gene targets such asB. anthracisprotective antigen (pagA, also called BAPA, occurring on plasmid pXO1), lethal factor (lef, on pXO1), capsule-encodingcapB/C(located on pXO2) as well as chromosomal Ba-1. Combinations of genetic markers using real-time/quantitative polymerase chain reaction (qPCR) are used to confirmB.anthracisfrom culture but can also be used directly on diagnostic samples to avoid propagation and its associated biorisks and for faster identification. We investigated how the presence of closely related species could complicate anthrax diagnoses with and without culture to standardise the use of genetic markers using qPCR for accurate anthrax diagnosis. Using blood smears from 2012–2020 from wildlife mortalities (n = 1708) in Kruger National Park in South Africa where anthrax is endemic, we contrasted anthrax diagnostic results based on qPCR, microscopy, and culture. From smears, 113/1708 grew bacteria in culture, from which 506 isolates were obtained. Of these isolates, only 24.7% (125 isolates) were positive forB.anthracisbased on genetic markers or microscopy. However, among these, merely 4/125 (3.2%) were confirmedB.anthracisisolates (based on morphology, microscopy, and sensitivity testing to penicillin and gamma-phage) from the blood smear, likely due to poor survival of spores on stored smears. This study identifiedB.cereus sensu lato, which includedB.cereusandB.anthracis,Peribacillusspp., andPriestiaspp. clusters usinggyrBgene in selected bacterial isolates positive forpagAregion using BAPA probe. Using qPCR on blood smears, 52.1% (890 samples) tested positive forB.anthracisbased on one or a combination of genetic markers which included the 25 positive controls. Notably, the standardlefprimer set displayed the lowest specificity and accuracy. The Ba-1+BAPA+lefcombination showed 100% specificity, sensitivity, and accuracy. Various marker combinations, such as Ba-1+capB, BAPA+capB, Ba-1+BAPA+capB+lef, and BAPA+lef+capB, all demonstrated 100.0% specificity and 98.7% accuracy, while maintaining a sensitivity of 96.6%. Using Ba-1+BAPA+lef+capB, as well as Ba-1+BAPA+lefwith molecular diagnosis accurately detectsB.anthracisin the absence of bacterial culture. Systematically combining microscopy and molecular markers holds promise for notably reducing false positives. This significantly enhances the detection and surveillance of diseases like anthrax in southern Africa and beyond and reduces the need for propagation of the bacteria in culture. 

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