Evidence for Loss of a Partial Flagellar Glycolytic Pathway during Trypanosomatid Evolution
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{"title"=>"Evidence for loss of a partial flagellar glycolytic pathway during trypanosomatid evolution", "type"=>"journal", "authors"=>[{"first_name"=>"Robert W B", "last_name"=>"Brown", "scopus_author_id"=>"56977060600"}, {"first_name"=>"Peter W.", "last_name"=>"Collingridge", "scopus_author_id"=>"35738353300"}, {"first_name"=>"Keith", "last_name"=>"Gull", "scopus_author_id"=>"7004312188"}, {"first_name"=>"Daniel J.", "last_name"=>"Rigden", "scopus_author_id"=>"7005750773"}, {"first_name"=>"Michael L.", "last_name"=>"Ginger", "scopus_author_id"=>"6602864622"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0103026", "issn"=>"19326203", "sgr"=>"84904703495", "scopus"=>"2-s2.0-84904703495", "pui"=>"373596096", "pmid"=>"25050549"}, "id"=>"2906279f-6f46-3576-a7ef-d8a41c30e7a6", "abstract"=>"Classically viewed as a cytosolic pathway, glycolysis is increasingly recognized as a metabolic pathway exhibiting surprisingly wide-ranging variations in compartmentalization within eukaryotic cells. Trypanosomatid parasites provide an extreme view of glycolytic enzyme compartmentalization as several glycolytic enzymes are found exclusively in peroxisomes. Here, we characterize Trypanosoma brucei flagellar proteins resembling glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and phosphoglycerate kinase (PGK): we show the latter associates with the axoneme and the former is a novel paraflagellar rod component. The paraflagellar rod is an essential extra-axonemal structure in trypanosomes and related protists, providing a platform into which metabolic activities can be built. Yet, bioinformatics interrogation and structural modelling indicate neither the trypanosome PGK-like nor the GAPDH-like protein is catalytically active. Orthologs are present in a free-living ancestor of the trypanosomatids, Bodo saltans: the PGK-like protein from B. saltans also lacks key catalytic residues, but its GAPDH-like protein is predicted to be catalytically competent. We discuss the likelihood that the trypanosome GAPDH-like and PGK-like proteins constitute molecular evidence for evolutionary loss of a flagellar glycolytic pathway, either as a consequence of niche adaptation or the re-localization of glycolytic enzymes to peroxisomes and the extensive changes to glycolytic flux regulation that accompanied this re-localization. Evidence indicating loss of localized ATP provision via glycolytic enzymes therefore provides a novel contribution to an emerging theme of hidden diversity with respect to compartmentalization of the ubiquitous glycolytic pathway in eukaryotes. A possibility that trypanosome GAPDH-like protein additionally represents a degenerate example of a moonlighting protein is also discussed.", "link"=>"http://www.mendeley.com/research/evidence-loss-partial-flagellar-glycolytic-pathway-during-trypanosomatid-evolution", "reader_count"=>22, "reader_count_by_academic_status"=>{"Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>5, "Student > Master"=>1, "Other"=>2, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>5, "Student > Master"=>1, "Other"=>2, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Business, Management and Accounting"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Argentina"=>1, "Czech Republic"=>1, "United Kingdom"=>1, "France"=>3}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1604951"], "description"=>"<p>(<b>A</b>) Indirect immunofluorescence using monoclonal antibody BB2 reveals axonemal localization of Ty::<i>Tb</i>PGKL in detergent-extracted procyclic <i>T. brucei</i> cytoskeletons. Cytoskeletons were stained with 4′,6-diamidino-2-phenylindole (DAPI) to detect mitochondrial (kinetoplast, K) and nuclear (N) DNA. The inset shows how the indirect immunofluorescence signal extends close to the kinetoplast, consistent with axoneme association. Scale bar denotes 5 µm. (<b>B</b>) Immunoblot analysis of detergent- and NaCl-extracted flagella isolated from procyclic cells expressing Ty::<i>Tb</i>PGK-like protein using BB2 detects a single band of the expected molecular mass.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "localization"], "article_id"=>1114238, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.g004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Flagellar_localization_of_Tb_PGKL_/1114238", "title"=>"Flagellar localization of <i>Tb</i>PGKL.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-22 03:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1604948"], "description"=>"<p>The representation is colored according to sequence conservation (blue-red, low to high) by Consurf. The catalytic Cys residue, neighboring residues (white sticks) and bound ligands (covalently attached glyceraldehyde-3-phosphate and NAD; ball and stick) from superimposed <i>G. stearothermophilus</i> GAPDH (PDB code 3cmc) are shown, with H-bonds illustrated as dotted lines. Corresponding residues in the TbGAPDHL model (purple sticks) are functionally incapable. Residues are labelled as template/model.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "tbgapdhl"], "article_id"=>1114235, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Surface_representation_of_TbGAPDHL_with_substrates_/1114235", "title"=>"Surface representation of TbGAPDHL with substrates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-22 03:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1604956"], "description"=>"<p>(<b>A</b>) Localization of GFP::<i>Tb</i>GAPDHL in procyclic <i>T. brucei</i> cells. (<b>B</b>) Indirect immunofluorescence of detergent-extracted cytoskeletons using the monoclonal antibody L8C4 to detect the major PFR protein PFR2 suggests GFP::<i>Tb</i>GAPDHL is a novel PFR component. Insets 1 and 2 indicate that at the proximal end of the flagellum PFR2 incorporation into flagellar skeleton does not begin prior to GFP::<i>Tb</i>GAPDHL incorporation – <i>cf</i> inset 2 in (<b>C</b>). (<b>C</b>) A lack of co-localization in indirect immunofluorescence of cytoskeletons using the monoclonal antibody L3B2 indicates GFP::<i>Tb</i>GAPDHL is not a cytoplasmic FAZ component: inset 1 indicates flagellar GFP::<i>Tb</i>GAPDHL fluorescence extends beyond the end of the cell body as denoted by L3B2 labelling of the cytoplasmic FAZ filament; inset 2 highlights how assembly the cytoplasmic FAZ filament detected by L3B2 initiates before assembly of GFP::<i>Tb</i>GAPDHL into the flagellar architecture. (<b>D</b>) Change in YFP::<i>Tb</i>GAPDHL localization in Tb<i>CaM</i> RNAi mutants: following RNAi induction and failure of PFR assembly YFP::<i>Tb</i>GAPDHL co-localizes with aggregates containing PFR2 protein (detected by indirect immunofluorescence with monoclonal antibody L8C4). (<b>E</b>) PFR localization of GFP::<i>Tb</i>GAPDHL is retained in <i>snl-2</i> RNAi mutants; detergent extracted cytoskeletons were also stained for indirect immunofluorescence with L13D6 to highlight failure to incorporate either PFR1 or PFR2, the two major PFR components, into the flagellar architecture. DIC, differential interference contrast; N, nucleus; K, kinetoplast. Scale bars denote 5 µm.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "localization"], "article_id"=>1114243, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PFR_localization_of_Tb_GAPDHL_/1114243", "title"=>"PFR localization of <i>Tb</i>GAPDHL.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-22 03:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1604950"], "description"=>"<p>(<b>A</b>) Cartoon schematic illustrating the modular architecture of TbPGKL. Positions of the predicted membrane-spanning helices are shown as vertical black bars; the additional helix predicted by Phobius is denoted by the grey vertical bar. (<b>B</b>) Comparison of the <i>Tb</i>PGKL ‘PGK’ domain model and the <i>T. brucei</i> PGK template structure (PDB code 13 pk; <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0103026#pone.0103026-Bernstein1\" target=\"_blank\">[56]</a>) in the vicinity of the catalytic site. The template is shown as white cartoon with key binding residues shown as sticks. Bound ligands (ADP, 3-phosphoglycerate) are shown as ball-and-stick, bound Mg<sup>2+</sup> as a grey sphere: their hydrogen bonds with the protein are shown as dotted lines. The model cartoon is colored from blue to red (N- to C-terminus) and equivalent residues to those shown for the template as purple sticks. Residues are labelled as template/model. In a few cases there is no equivalent model residue due to deletions in the alignment. (<b>C</b>) Comparison of the <i>Tb</i>PGKL post-‘PGK’ domains model and the <i>T. thermophilus</i> CRP template structure (PDB code 4ev0; unpublished) in the vicinity of the cAMP binding site. The template is shown as white cartoon with key binding residues shown as sticks. Bound cAMP is shown as ball-and-stick: its hydrogen bonds with the protein are shown as dotted lines. The model cartoon is colored from blue to red (N- to C-terminus) and equivalent residues to those shown for the template as purple sticks. Residues are labelled as template/model.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "pgkl"], "article_id"=>1114237, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.g003", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modular_architecture_and_modelling_of_T_brucei_PGKL_proteins_/1114237", "title"=>"Modular architecture and modelling of <i>T. brucei</i> PGKL proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-22 03:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1604946"], "description"=>"<p>The alignment was built using MUSCLE and sequences are named with species abbreviations (Tb =  <i>T. brucei</i>, Tc =  <i>T. cruzi</i>, Lm =  <i>L. major</i>, Bs =  <i>B. saltans</i>, Gt =  <i>Geobacillus stearothermophilus</i>, Mb =  <i>Mycobacterium bovis</i>, Hs =  <i>Homo sapiens</i>, Ce =  <i>Caenorhabditis elegans</i>, Mj =  <i>Methanocaldococcus jannaschii</i>, Pt =  <i>Picrophilus torridus</i>) followed by a locus code (kinetoplastid sequences) or UniProt accession. For kinetoplastid sequences, cGAPDH indicates the cytosolic isoform and gGAPDH the glycosomal enzyme. Only one each of the tandem copies of gGAPDH is shown for each trypanosomatid. Residues mentioned in the text are highlighted as white on purple.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "alignment", "trypanosomatid", "gapdhl", "proteins", "authentic"], "article_id"=>1114233, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.g001", "stats"=>{"downloads"=>7, "page_views"=>103, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_alignment_of_trypanosomatid_GAPDHL_proteins_with_authentic_GAPDH_/1114233", "title"=>"Sequence alignment of trypanosomatid GAPDHL proteins with authentic GAPDH.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-22 03:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1604958"], "description"=>"<p>Each group contains sequences (eliminating tandem duplicates) from <i>T. brucei, T. cruzi, T. vivax, L. braziliensis, L. mexicana, L. major, L. infantum, L. tarentolae</i>, and <i>Endotrypanum monterogeii</i>.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "amino", "identities", "groups"], "article_id"=>1114245, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.t001", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Range_and_mean_percentage_amino_acid_identities_between_GAPDH_like_groups_in_trypanosomatids_/1114245", "title"=>"Range and mean percentage amino acid identities between GAPDH(-like) groups in trypanosomatids.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-07-22 03:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/1604957"], "description"=>"<p>(<b>A</b>) Generation of Tb<i>GAPDHL</i> null mutants. (<b>B</b>) Generation of Tb<i>PGKL</i> null mutants. Cartoon schematics denote gene loci annotated with HindIII (H) restriction sites for (i) wild-type loci; (ii) loci following gene disruption and (iii) following endogenous gene-tagging with GFP (Tb<i>GAPDHL</i> only). Southern analysis of genomic DNA digested overnight at 37°C with HindIII shows blots probed sequentially with either coding sequence from the targeted gene (probe o) or sequence from the 3′ intergenic region (probe u). Relative positions of the probes are shown in the cartoon schematics. In (<b>A</b>) the order of lanes is 1, wild-type <i>GAPDHL</i><sup>+/+</sup><i>T. brucei</i>; 2, heterozygous <i>GAPDHL</i><sup>+/−</sup> cells resistant to phleomycin; 3, heterozygous <i>GAPDHL</i><sup>+/−</sup> cells resistant to blasticidin/HCl; 4-5, <i>GAPDHL</i><sup>+/−</sup> heterozygotes from lanes 2 and 3, respectively, in which endogenous tagging of the remaining wild-type allele results in expression of a recombinant e<i>GFP:GAPDHL</i>; 6, a <i>GAPDHL<sup>−/−</sup></i> mutant obtained from the stable transformation of the phleomycin-resistant heterozygote cells from lane 2. In (<b>B</b>) the order of lanes is 1, wild-type <i>PGKL</i><sup>+/+</sup>, 2, heterozygous <i>GAPDHL</i><sup>+/−</sup> cells resistant to phleomycin; 3, heterozygous <i>GAPDHL</i><sup>+/−</sup> cells resistant to blasticidin/HCl; 4–5, independently obtained <i>PGKL</i><sup>−/−</sup> mutants derived from the stable transformation of heterozygous cell lines analyzed in lanes 2 and 3, respectively.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Carbohydrate metabolism", "Glucose metabolism", "cell biology", "Cellular structures and organelles", "cilia", "Subcellular localization", "Evolutionary biology", "Evolutionary processes", "Evolutionary adaptation", "microbiology", "Protozoology", "Kinetoplastids", "Parasitology", "Parasite physiology", "procyclic", "null"], "article_id"=>1114244, "categories"=>["Biological Sciences"], "users"=>["Robert W. B. Brown", "Peter W. Collingridge", "Keith Gull", "Daniel J. Rigden", "Michael L. Ginger"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103026.g006", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Generation_of_Tb_GAPDHL_and_Tb_PGKL_procyclic_null_mutants_/1114244", "title"=>"Generation of Tb<i>GAPDHL</i> and Tb<i>PGKL</i> procyclic null mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-22 03:01:41"}

PMC Usage Stats | Further Information

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Relative Metric

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