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Genome and phylogenetic analyses of Trypanosoma evansi reveal extensive similarity to T. brucei and multiple independent origins for dyskinetoplasty.

Carnes J, Anupama A, Balmer O, Jackson A, Lewis M, Brown R, Cestari I, Desquesnes M, Gendrin C, Hertz-Fowler C, Imamura H, Ivens A, Kořený L, Lai DH, MacLeod A, McDermott SM, Merritt C, Monnerat S, Moon W, Myler P, Phan I, Ramasamy G, Sivam D, Lun ZR, Lukeš J, Stuart K, Schnaufer A - PLoS Negl Trop Dis (2015)

Bottom Line: Surprisingly, orthologous sequences were found in T. evansi for all 978 nuclear CDS predicted to represent the mitochondrial proteome in T. brucei, although a small number of these may have lost functionality.Consistent with previous results, the F1FO-ATP synthase γ subunit was found to have an A281 deletion, which is involved in generation of a mitochondrial membrane potential in the absence of kDNA.Overall, the elucidation of the T. evansi genome sequence reveals extensive similarity of T. brucei and supports the contention that T. evansi should be classified as a subspecies of T. brucei.

View Article: PubMed Central - PubMed

Affiliation: Seattle Biomedical Research Institute, Seattle, United States of America.

ABSTRACT
Two key biological features distinguish Trypanosoma evansi from the T. brucei group: independence from the tsetse fly as obligatory vector, and independence from the need for functional mitochondrial DNA (kinetoplast or kDNA). In an effort to better understand the molecular causes and consequences of these differences, we sequenced the genome of an akinetoplastic T. evansi strain from China and compared it to the T. b. brucei reference strain. The annotated T. evansi genome shows extensive similarity to the reference, with 94.9% of the predicted T. b. brucei coding sequences (CDS) having an ortholog in T. evansi, and 94.6% of the non-repetitive orthologs having a nucleotide identity of 95% or greater. Interestingly, several procyclin-associated genes (PAGs) were disrupted or not found in this T. evansi strain, suggesting a selective loss of function in the absence of the insect life-cycle stage. Surprisingly, orthologous sequences were found in T. evansi for all 978 nuclear CDS predicted to represent the mitochondrial proteome in T. brucei, although a small number of these may have lost functionality. Consistent with previous results, the F1FO-ATP synthase γ subunit was found to have an A281 deletion, which is involved in generation of a mitochondrial membrane potential in the absence of kDNA. Candidates for CDS that are absent from the reference genome were identified in supplementary de novo assemblies of T. evansi reads. Phylogenetic analyses show that the sequenced strain belongs to a dominant group of clonal T. evansi strains with worldwide distribution that also includes isolates classified as T. equiperdum. At least three other types of T. evansi or T. equiperdum have emerged independently. Overall, the elucidation of the T. evansi genome sequence reveals extensive similarity of T. brucei and supports the contention that T. evansi should be classified as a subspecies of T. brucei.

No MeSH data available.


Related in: MedlinePlus

Bayesian phylogeny of Trypanozoon isolates based on the dihydrolipoamide dehydrogenase gene (LipDH; Tb927.11.16730).Panel A shows a mid-point rooted tree based on an alignment of 32 unique LipDH haplotypes, assembled from sequences derived from 13 T. b. brucei (Tbb), 3 T. b. gambiense type 1 (Tbg1), 4 T. b. rhodesiense (Tbr), 15 T. evansi (Tev) and 5 T. equiperdum (Teq) samples. Scale units for the phylogeny are substitutions per site. The chart illustrates the distribution of each haplotype among samples from each Trypanozoon taxon. Phylogenetic analysis grouped all but three of the haplotype sequences into one of five major clusters with strong support (posterior probabilities ≥0.9), which are referred to as clades V, W, X, Y and Z. Eight unique Tev/Teq genotypes were found, as summarized in panel B. Discounting minor sequence differences (1–2 SNPs) these were reduced to four major genotypes based on the position of haplotypes in the tree, which mirrored the type of mutation (A281Δ, M282L, A273P, WT) in the C-termini of the ATP synthase subunit γ in these the samples.
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pntd-0003404-g005: Bayesian phylogeny of Trypanozoon isolates based on the dihydrolipoamide dehydrogenase gene (LipDH; Tb927.11.16730).Panel A shows a mid-point rooted tree based on an alignment of 32 unique LipDH haplotypes, assembled from sequences derived from 13 T. b. brucei (Tbb), 3 T. b. gambiense type 1 (Tbg1), 4 T. b. rhodesiense (Tbr), 15 T. evansi (Tev) and 5 T. equiperdum (Teq) samples. Scale units for the phylogeny are substitutions per site. The chart illustrates the distribution of each haplotype among samples from each Trypanozoon taxon. Phylogenetic analysis grouped all but three of the haplotype sequences into one of five major clusters with strong support (posterior probabilities ≥0.9), which are referred to as clades V, W, X, Y and Z. Eight unique Tev/Teq genotypes were found, as summarized in panel B. Discounting minor sequence differences (1–2 SNPs) these were reduced to four major genotypes based on the position of haplotypes in the tree, which mirrored the type of mutation (A281Δ, M282L, A273P, WT) in the C-termini of the ATP synthase subunit γ in these the samples.

Mentions: 32 unique LipDH haplotypes were identified. The majority of strains (36/41) had two different alleles and four strains appeared to be homozygous at this locus, all of which were T. b. brucei (although it cannot be ruled out that the primers used were selective for one allele in these cases). Phylogenetic analysis (Fig. 5) showed all but three of the haplotype sequences fell into one of five major clusters with strong support (posterior probabilities ≥0.9), which we refer to as clades V, W, X, Y and Z. Importantly, 14 different haplotypes are derived from the T. evansi/T. equiperdum isolates, which are found in three different clades as well as outside of the clades. This feature is incompatible with monophyly of T. evansi or T. equiperdum. Some subspecies did have relatively restricted phylogenetic diversity, for example T. b. gambiense type 1 had only five closely related haplotypes and certain clades contained sequences from a restricted number of the subspecies; e.g. clade X only contained T. b. rhodesiense and T. b. brucei; clade Y included only T. b. gambiense type 1 and T. b. brucei. This may reflect relatively more recent origins of certain populations, bottleneck events and/or sampling bias, and is in line with most previous work ([40] and references therein).


Genome and phylogenetic analyses of Trypanosoma evansi reveal extensive similarity to T. brucei and multiple independent origins for dyskinetoplasty.

Carnes J, Anupama A, Balmer O, Jackson A, Lewis M, Brown R, Cestari I, Desquesnes M, Gendrin C, Hertz-Fowler C, Imamura H, Ivens A, Kořený L, Lai DH, MacLeod A, McDermott SM, Merritt C, Monnerat S, Moon W, Myler P, Phan I, Ramasamy G, Sivam D, Lun ZR, Lukeš J, Stuart K, Schnaufer A - PLoS Negl Trop Dis (2015)

Bayesian phylogeny of Trypanozoon isolates based on the dihydrolipoamide dehydrogenase gene (LipDH; Tb927.11.16730).Panel A shows a mid-point rooted tree based on an alignment of 32 unique LipDH haplotypes, assembled from sequences derived from 13 T. b. brucei (Tbb), 3 T. b. gambiense type 1 (Tbg1), 4 T. b. rhodesiense (Tbr), 15 T. evansi (Tev) and 5 T. equiperdum (Teq) samples. Scale units for the phylogeny are substitutions per site. The chart illustrates the distribution of each haplotype among samples from each Trypanozoon taxon. Phylogenetic analysis grouped all but three of the haplotype sequences into one of five major clusters with strong support (posterior probabilities ≥0.9), which are referred to as clades V, W, X, Y and Z. Eight unique Tev/Teq genotypes were found, as summarized in panel B. Discounting minor sequence differences (1–2 SNPs) these were reduced to four major genotypes based on the position of haplotypes in the tree, which mirrored the type of mutation (A281Δ, M282L, A273P, WT) in the C-termini of the ATP synthase subunit γ in these the samples.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4288722&req=5

pntd-0003404-g005: Bayesian phylogeny of Trypanozoon isolates based on the dihydrolipoamide dehydrogenase gene (LipDH; Tb927.11.16730).Panel A shows a mid-point rooted tree based on an alignment of 32 unique LipDH haplotypes, assembled from sequences derived from 13 T. b. brucei (Tbb), 3 T. b. gambiense type 1 (Tbg1), 4 T. b. rhodesiense (Tbr), 15 T. evansi (Tev) and 5 T. equiperdum (Teq) samples. Scale units for the phylogeny are substitutions per site. The chart illustrates the distribution of each haplotype among samples from each Trypanozoon taxon. Phylogenetic analysis grouped all but three of the haplotype sequences into one of five major clusters with strong support (posterior probabilities ≥0.9), which are referred to as clades V, W, X, Y and Z. Eight unique Tev/Teq genotypes were found, as summarized in panel B. Discounting minor sequence differences (1–2 SNPs) these were reduced to four major genotypes based on the position of haplotypes in the tree, which mirrored the type of mutation (A281Δ, M282L, A273P, WT) in the C-termini of the ATP synthase subunit γ in these the samples.
Mentions: 32 unique LipDH haplotypes were identified. The majority of strains (36/41) had two different alleles and four strains appeared to be homozygous at this locus, all of which were T. b. brucei (although it cannot be ruled out that the primers used were selective for one allele in these cases). Phylogenetic analysis (Fig. 5) showed all but three of the haplotype sequences fell into one of five major clusters with strong support (posterior probabilities ≥0.9), which we refer to as clades V, W, X, Y and Z. Importantly, 14 different haplotypes are derived from the T. evansi/T. equiperdum isolates, which are found in three different clades as well as outside of the clades. This feature is incompatible with monophyly of T. evansi or T. equiperdum. Some subspecies did have relatively restricted phylogenetic diversity, for example T. b. gambiense type 1 had only five closely related haplotypes and certain clades contained sequences from a restricted number of the subspecies; e.g. clade X only contained T. b. rhodesiense and T. b. brucei; clade Y included only T. b. gambiense type 1 and T. b. brucei. This may reflect relatively more recent origins of certain populations, bottleneck events and/or sampling bias, and is in line with most previous work ([40] and references therein).

Bottom Line: Surprisingly, orthologous sequences were found in T. evansi for all 978 nuclear CDS predicted to represent the mitochondrial proteome in T. brucei, although a small number of these may have lost functionality.Consistent with previous results, the F1FO-ATP synthase γ subunit was found to have an A281 deletion, which is involved in generation of a mitochondrial membrane potential in the absence of kDNA.Overall, the elucidation of the T. evansi genome sequence reveals extensive similarity of T. brucei and supports the contention that T. evansi should be classified as a subspecies of T. brucei.

View Article: PubMed Central - PubMed

Affiliation: Seattle Biomedical Research Institute, Seattle, United States of America.

ABSTRACT
Two key biological features distinguish Trypanosoma evansi from the T. brucei group: independence from the tsetse fly as obligatory vector, and independence from the need for functional mitochondrial DNA (kinetoplast or kDNA). In an effort to better understand the molecular causes and consequences of these differences, we sequenced the genome of an akinetoplastic T. evansi strain from China and compared it to the T. b. brucei reference strain. The annotated T. evansi genome shows extensive similarity to the reference, with 94.9% of the predicted T. b. brucei coding sequences (CDS) having an ortholog in T. evansi, and 94.6% of the non-repetitive orthologs having a nucleotide identity of 95% or greater. Interestingly, several procyclin-associated genes (PAGs) were disrupted or not found in this T. evansi strain, suggesting a selective loss of function in the absence of the insect life-cycle stage. Surprisingly, orthologous sequences were found in T. evansi for all 978 nuclear CDS predicted to represent the mitochondrial proteome in T. brucei, although a small number of these may have lost functionality. Consistent with previous results, the F1FO-ATP synthase γ subunit was found to have an A281 deletion, which is involved in generation of a mitochondrial membrane potential in the absence of kDNA. Candidates for CDS that are absent from the reference genome were identified in supplementary de novo assemblies of T. evansi reads. Phylogenetic analyses show that the sequenced strain belongs to a dominant group of clonal T. evansi strains with worldwide distribution that also includes isolates classified as T. equiperdum. At least three other types of T. evansi or T. equiperdum have emerged independently. Overall, the elucidation of the T. evansi genome sequence reveals extensive similarity of T. brucei and supports the contention that T. evansi should be classified as a subspecies of T. brucei.

No MeSH data available.


Related in: MedlinePlus