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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

Maximum parsimony haplotype network showing phylogenetic relationships among Trypanozoon haplotypes using cytochrome oxidase 1 (COX1).Relationships among lineages of T. b. brucei (blue), T. b. rhodesiense (red), T. b. gambiense group 1 (dark green) and T. b. gambiense group 2 (light green) are shown in circles as in reference [40], with haplotypes new to this study shown as octagons, including two new haplotypes for T. equiperdum isolates (pink). The size of each circle or octagon is proportional to the frequency with which a particular haplotype was identified. Numbers in the circles and octagons correspond to haplotype ID. Empty circles indicate haplotypes that are inferred to exist but were not found. The light blue boxes correspond to the T. brucei clades defined in [40]. Haplotypes for samples new to this study are as follows (from left to right): 8 =  Tbg14; 5 =  Tbr01/Tbr04; 20 =  Tbb49/Tbb50; 21 =  Tbb51; 3 =  Tbb20; 2 =  Tbb38; 23 =  Teq24; 14 =  Tbr02/Teq23; 22 =  Teq21/Teq22.
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pntd-0003404-g006: Maximum parsimony haplotype network showing phylogenetic relationships among Trypanozoon haplotypes using cytochrome oxidase 1 (COX1).Relationships among lineages of T. b. brucei (blue), T. b. rhodesiense (red), T. b. gambiense group 1 (dark green) and T. b. gambiense group 2 (light green) are shown in circles as in reference [40], with haplotypes new to this study shown as octagons, including two new haplotypes for T. equiperdum isolates (pink). The size of each circle or octagon is proportional to the frequency with which a particular haplotype was identified. Numbers in the circles and octagons correspond to haplotype ID. Empty circles indicate haplotypes that are inferred to exist but were not found. The light blue boxes correspond to the T. brucei clades defined in [40]. Haplotypes for samples new to this study are as follows (from left to right): 8 =  Tbg14; 5 =  Tbr01/Tbr04; 20 =  Tbb49/Tbb50; 21 =  Tbb51; 3 =  Tbb20; 2 =  Tbb38; 23 =  Teq24; 14 =  Tbr02/Teq23; 22 =  Teq21/Teq22.

Mentions: The COX1 gene, encoded in the mitochondrial maxicircle DNA, was recently used as a highly informative marker to investigate the phylogeography of T. brucei subspecies [40]. Although most, if not all, T. evansi isolates lack a maxicircle, the presence of at least one T. equiperdum isolate with at least a partial maxicircle in three of the above groups prompted us to determine the COX1 haplotypes for these strains and to investigate their relationship with the Trypanozoon isolates from the earlier study (S7 Table). A maximum parsimony network analysis strongly supported the notion of three independent evolutionary origins for these three groups (Fig. 6). T. equiperdum STIB818 (Teq24; COX1 haplotype 23) links Group 1 with COX1 clade A, which is composed of isolates of all three T. brucei subspecies found across all of sub-Saharan Africa [40]. Although Groups 2 and 3, which share a related ‘V’ LipDH genotype, are both linked to COX1 clade C (composed of T. b. brucei and T. b. rhodesiense isolates from eastern and southern Africa), they are well separated within this clade, indicating independent evolutionary origins. T. equiperdum STIB841 (Teq23) shares both its COX1 haplotype 14 and its LipDH haplotype 19 with Tbr02 from Zambia and Tbb08 from Kenya, both members of the Kiboko group, suggesting relatively recent common ancestry. Note that Tev42 (KETRI2479), the lone representative of the ‘atypical’ LipDH genotype, is not represented in this network since this isolate lacks a maxicircle and therefore the COX1 gene.


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)

Maximum parsimony haplotype network showing phylogenetic relationships among Trypanozoon haplotypes using cytochrome oxidase 1 (COX1).Relationships among lineages of T. b. brucei (blue), T. b. rhodesiense (red), T. b. gambiense group 1 (dark green) and T. b. gambiense group 2 (light green) are shown in circles as in reference [40], with haplotypes new to this study shown as octagons, including two new haplotypes for T. equiperdum isolates (pink). The size of each circle or octagon is proportional to the frequency with which a particular haplotype was identified. Numbers in the circles and octagons correspond to haplotype ID. Empty circles indicate haplotypes that are inferred to exist but were not found. The light blue boxes correspond to the T. brucei clades defined in [40]. Haplotypes for samples new to this study are as follows (from left to right): 8 =  Tbg14; 5 =  Tbr01/Tbr04; 20 =  Tbb49/Tbb50; 21 =  Tbb51; 3 =  Tbb20; 2 =  Tbb38; 23 =  Teq24; 14 =  Tbr02/Teq23; 22 =  Teq21/Teq22.
© Copyright Policy
Related In: Results  -  Collection

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

pntd-0003404-g006: Maximum parsimony haplotype network showing phylogenetic relationships among Trypanozoon haplotypes using cytochrome oxidase 1 (COX1).Relationships among lineages of T. b. brucei (blue), T. b. rhodesiense (red), T. b. gambiense group 1 (dark green) and T. b. gambiense group 2 (light green) are shown in circles as in reference [40], with haplotypes new to this study shown as octagons, including two new haplotypes for T. equiperdum isolates (pink). The size of each circle or octagon is proportional to the frequency with which a particular haplotype was identified. Numbers in the circles and octagons correspond to haplotype ID. Empty circles indicate haplotypes that are inferred to exist but were not found. The light blue boxes correspond to the T. brucei clades defined in [40]. Haplotypes for samples new to this study are as follows (from left to right): 8 =  Tbg14; 5 =  Tbr01/Tbr04; 20 =  Tbb49/Tbb50; 21 =  Tbb51; 3 =  Tbb20; 2 =  Tbb38; 23 =  Teq24; 14 =  Tbr02/Teq23; 22 =  Teq21/Teq22.
Mentions: The COX1 gene, encoded in the mitochondrial maxicircle DNA, was recently used as a highly informative marker to investigate the phylogeography of T. brucei subspecies [40]. Although most, if not all, T. evansi isolates lack a maxicircle, the presence of at least one T. equiperdum isolate with at least a partial maxicircle in three of the above groups prompted us to determine the COX1 haplotypes for these strains and to investigate their relationship with the Trypanozoon isolates from the earlier study (S7 Table). A maximum parsimony network analysis strongly supported the notion of three independent evolutionary origins for these three groups (Fig. 6). T. equiperdum STIB818 (Teq24; COX1 haplotype 23) links Group 1 with COX1 clade A, which is composed of isolates of all three T. brucei subspecies found across all of sub-Saharan Africa [40]. Although Groups 2 and 3, which share a related ‘V’ LipDH genotype, are both linked to COX1 clade C (composed of T. b. brucei and T. b. rhodesiense isolates from eastern and southern Africa), they are well separated within this clade, indicating independent evolutionary origins. T. equiperdum STIB841 (Teq23) shares both its COX1 haplotype 14 and its LipDH haplotype 19 with Tbr02 from Zambia and Tbb08 from Kenya, both members of the Kiboko group, suggesting relatively recent common ancestry. Note that Tev42 (KETRI2479), the lone representative of the ‘atypical’ LipDH genotype, is not represented in this network since this isolate lacks a maxicircle and therefore the COX1 gene.

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