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Phylogeography and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports.

ABSTRACT: Pathology to vertebrate hosts has emerged repeatedly in the order Ophiostomatales. Occasional infections have been observed in Sporothrix mexicana at a low level of virulence, while the main pathogenic species cluster in a derived clade around S. schenckii s.str. In this paper, phylogeny and epidemiology of the members of this clade were investigated for 99 clinical and 36 environmental strains using four genetic loci, viz. rDNA ITS and partial CAL, TEF1, and TEF3; data are compared with amplified fragment length polymorphism (AFLP) genotyping. The four main species of the pathogenic clade were recognised. The species proved to show high degrees of endemicity, which enabled interpretation of literature data where live material or genetic information is lacking. The clade of four species comprised nine subclusters, which often had limited geographic distribution and were separate from each other in all partitions, suggesting low degrees of interbreeding between populations. In contrast, S. globosa exhibited consistent global distribution of identical AFLP types, suggesting another type of dispersal. Sporothrix brasiliensis is known to be involved in an expanding zoonosis and transmitted by cats, whereas S. globosa infections originated from putrid plant material, causing a sapronosis. Sporothrix schenckii s.str., the most variable species within the clade, also had a plant origin, with ecological similarities to that of S. globosa. A hypothesis was put forward that highly specific conditions in the plant material are required to promote the growth of Sporothrix. Fermented, self-heated plant debris may stimulate the thermodependent yeast-like invasive form of the fungus, which facilitates repeated infection of mammals.

SUBMITTER: Zhang Y

PROVIDER: S-EPMC4713101 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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Phylogeography and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports.

Zhang Y Y Hagen F F Stielow B B Rodrigues A M AM Samerpitak K K Zhou X X Feng P P Yang L L Chen M M Deng S S Li S S Liao W W Li R R Li F F Meis J F JF Guarro J J Teixeira M M Al-Zahrani H S HS Pires de Camargo Z Z Zhang L L de Hoog G S GS

Persoonia 20150129

Pathology to vertebrate hosts has emerged repeatedly in the order Ophiostomatales. Occasional infections have been observed in Sporothrix mexicana at a low level of virulence, while the main pathogenic species cluster in a derived clade around S. schenckii s.str. In this paper, phylogeny and epidemiology of the members of this clade were investigated for 99 clinical and 36 environmental strains using four genetic loci, viz. rDNA ITS and partial CAL, TEF1, and TEF3; data are compared with amplifi ...[more]

PMID: 26823625

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Project description:BackgroundThe genus Sporothrix belongs to the order Ophiostomatales and contains mainly saprobic soil and plant fungi, although pathogenic species capable of causing human infections are also present. The whole-genomes of disease-causing species have already been sequenced and annotated but no comprehensive genomic resources for environmental Sporothrix species are available, thus limiting our understanding of the evolutionary origin of virulence-related genes and pathogenicity.ResultThe genome assembly of four environmental Sporothrix species resulted in genome size of ~ 30.9 Mbp in Sporothrix phasma, ~ 35 Mbp in S. curviconia, ~ 38.7 Mbp in S. protearum, and ~ 39 Mbp in S. variecibatus, with a variable gene content, ranging from 8142 (S. phasma) to 9502 (S. variecibatus). The analysis of mobile genetic elements showed significant differences in the content of transposable elements within the sequenced genomes, with the genome of S. phasma lacking several class I and class II transposons, compared to the other Sporothrix genomes investigated. Moreover, the comparative analysis of orthologous genes shared by clinical and environmental Sporothrix genomes revealed the presence of 3622 orthogroups shared by all species, whereas over 4200 genes were species-specific single-copy gene products. Carbohydrate-active enzyme analysis revealed a total of 2608 protein-coding genes containing single and/or multiple CAZy domains, resulting in no statistically significant differences among pathogenic and environmental species. Nevertheless, some families were not found in clinical species. Furthermore, for each sequenced Sporothrix species, the mitochondrial genomes was assembled in a single circular DNA molecule, ranging from 25,765 bp (S. variecibatus) to 58,395 bp (S. phasma).ConclusionIn this study, we present four annotated genome assemblies generated using PacBio SMRT sequencing data from four environmental species: S. curviconia, S. phasma, S. protearum and S. variecibatus with the aim to provide a starting point for future comparative genome evolution studies addressing species diversification, ecological/host adaptation and origin of pathogenic lineages within the genus Sporothrix.

Project description:BACKGROUND: The fungal genus Sporothrix includes at least four human pathogenic species. One of these species, S. brasiliensis, is the causal agent of a major ongoing zoonotic outbreak of sporotrichosis in Brazil. Elsewhere, sapronoses are caused by S. schenckii and S. globosa. The major aims on this comparative genomic study are: 1) to explore the presence of virulence factors in S. schenckii and S. brasiliensis; 2) to compare S. brasiliensis, which is cat-transmitted and infects both humans and cats with S. schenckii, mainly a human pathogen; 3) to compare these two species to other human pathogens (Onygenales) with similar thermo-dimorphic behavior and to other plant-associated Sordariomycetes. RESULTS: The genomes of S. schenckii and S. brasiliensis were pyrosequenced to 17x and 20x coverage comprising a total of 32.3 Mb and 33.2 Mb, respectively. Pair-wise genome alignments revealed that the two species are highly syntenic showing 97.5% average sequence identity. Phylogenomic analysis reveals that both species diverged about 3.8-4.9 MYA suggesting a recent event of speciation. Transposable elements comprise respectively 0.34% and 0.62% of the S. schenckii and S. brasiliensis genomes and expansions of Gypsy-like elements was observed reflecting the accumulation of repetitive elements in the S. brasiliensis genome. Mitochondrial genomic comparisons showed the presence of group-I intron encoding homing endonucleases (HE's) exclusively in S. brasiliensis. Analysis of protein family expansions and contractions in the Sporothrix lineage revealed expansion of LysM domain-containing proteins, small GTPases, PKS type1 and leucin-rich proteins. In contrast, a lack of polysaccharide lyase genes that are associated with decay of plants was observed when compared to other Sordariomycetes and dimorphic fungal pathogens, suggesting evolutionary adaptations from a plant pathogenic or saprobic to an animal pathogenic life style. CONCLUSIONS: Comparative genomic data suggest a unique ecological shift in the Sporothrix lineage from plant-association to mammalian parasitism, which contributes to the understanding of how environmental interactions may shape fungal virulence. . Moreover, the striking differences found in comparison with other dimorphic fungi revealed that dimorphism in these close relatives of plant-associated Sordariomycetes is a case of convergent evolution, stressing the importance of this morphogenetic change in fungal pathogenesis.

Project description:BACKGROUND: Multiple loci and population genetic methods were employed to study the phylogeographic history of the Patagonian freshwater crab Aegla neuquensis (Aeglidae: Decopoda). This taxon occurs in two large river systems in the Patagonian Steppe, from the foothills of the Andes Mountains east to the Atlantic Ocean. METHODOLOGY/PRINCIPAL FINDINGS: A nuclear phylogeny and multilocus nested clade phylogeographic analysis detected a fragmentation event between the Negro and Chico-Chubut river systems. This event occurred approximately 137 thousand years ago. An isolation-with-migration analysis and maximum-likelihood estimates of gene flow showed asymmetrical exchange of genetic material between these two river systems exclusively in their headwaters. We used information theory to determine the best-fit demographic history between these two river systems under an isolation-with-migration model. The best-fit model suggests that the Negro and the ancestral populations have the same effective population sizes; whereas the Chico-Chubut population is smaller and shows that gene flow from the Chico-Chubut into the Negro is four times higher than in the reverse direction. Much of the Chico-Chubut system appears to have only been recently colonized while the Negro populations appear to have been in place for most of the evolutionary history of this taxon. CONCLUSIONS/SIGNIFICANCE: Due to mitochondrial introgression, three nuclear loci provided different phylogeographic resolution than the three mitochondrial genes for an ancient fragmentation event observed in the nuclear phylogeny. However, the mitochondrial locus provided greater resolution on more recent evolutionary events. Our study, therefore, demonstrates the need to include both nuclear and mitochondrial loci for a more complete understanding of evolutionary histories and associated phylogeographic events. Our results suggest that gene flow between these systems, before and after fragmentation was through periodic paleolakes that formed in the headwaters region. Fragmentation between the Negro and Chico-Chubut systems was driven by the disappearance of these paleolakes during the Patagonian Glaciation.

Project description:BackgroundAcross the tree of life there are numerous evolutionary transitions between different habitats (i.e., aquatic and terrestrial or marine and freshwater). Many of these dramatic evolutionary shifts parallel developmental shifts that require physiological, anatomical and behavioral changes for survival and reproduction. Diadromy (scheduled movement between marine and freshwater) has been characterized as a behavior that acts as an evolutionary intermediate state between marine and freshwater environments, implying that diadromous lineages are evolutionarily transient. This hypothesis comes with assumptions regarding the rates of evolutionary transitions in and out of diadromy as well as rates of speciation and extinction in diadromous fishes.ResultsBased on a published phylogeny of 7822 species of ray-finned fishes, state speciation and extinction models of evolutionary transition between marine, freshwater, and diadromous species suggest transition rates out of diadromy are 5-100 times higher that transition between marine and freshwater or into diadromy. Additionally, high speciation and low extinction rates separate diadromous fishes from marine and freshwater species. As a result, net diversification (net diversification = speciation - extinction) is about 7-40 times higher in diadromous fishes compared to freshwater and marine respectively. Together the transition, speciation, and extinction rates suggest diadromy is the least stable of the three states.ConclusionEvolutionary transitions to diadromy are rare in fishes. However, once established, diversification rates in diadromous lineages are high compared to both marine and freshwater species. Diadromous lineages tend to be more transient than marine or freshwater lineages and are found to give rise to marine and freshwater specialists in addition to diadromous descendants. Although diadromy is not a necessary evolutionary intermediate between marine and freshwater, these results support the interpretation of diadromy as an important, occasionally intermediate state, that contributes to biodiversity in fishes in all environments. This evolutionary instability of diadromous lineages is counteracted by their relatively high diversification rates. These findings highlight the importance of integrating the dynamics of diversification and major evolutionary transitions for understanding macroevolutionary patterns.

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Phylogeography and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports.

Publications

Phylogeography and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports.

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