Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-19T10:42:01.982Z Has data issue: false hasContentIssue false
  • English
  • Français

De novo synthesis of thiamine (vitamin B1) is the ancestral state in Plasmodium parasites – evidence from avian haemosporidians

Published online by Cambridge University Press:  12 December 2017

Olof Hellgren ,
Staffan Bensch  and
Elin Videvall
Olof Hellgren*
Affiliation:
MEMEG, Department of Biology, Lund University, Sölvegatan 37, 223 62 Lund, Sweden
Staffan Bensch
Affiliation:
MEMEG, Department of Biology, Lund University, Sölvegatan 37, 223 62 Lund, Sweden
Elin Videvall
Affiliation:
MEMEG, Department of Biology, Lund University, Sölvegatan 37, 223 62 Lund, Sweden
*
Author for correspondence: Olof Hellgren, Email: Olof.Hellgren@biol.lu.se
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasites often have reduced genomes as their own genes become redundant when utilizing their host as a source of metabolites, thus losing their own de novo production of metabolites. Primate malaria parasites can synthesize vitamin B1 (thiamine) de novo but rodent malaria and other genome-sequenced apicomplexans cannot, as the three essential genes responsible for this pathway are absent in their genomes. The unique presence of functional thiamine synthesis genes in primate malaria parasites and their sequence similarities to bacterial orthologues, have led to speculations that this pathway was horizontally acquired from bacteria. Here we show that the genes essential for the de novo synthesis of thiamine are found also in avian Plasmodium species. Importantly, they are also present in species phylogenetically basal to all mammalian and avian Plasmodium parasites, i.e. Haemoproteus. Furthermore, we found that these genes are expressed during the blood stage of the avian malaria infection, indicating that this metabolic pathway is actively transcribed. We conclude that the ability to synthesize thiamine is widespread among haemosporidians, with a recent loss in the rodent malaria species.

Keywords

Apicomplexaauxotrophyavian malariagene lossplasmodiumthiamine
Type
Research Article
Information
Parasitology , Volume 145 , Issue 8 , July 2018 , pp. 1084 - 1089
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aurrecoechea, C, Brestelli, J, Brunk, BP, Dommer, J, Fischer, S, Gajria, B, Gao, X, Gingle, A, Grant, G, Harb, OS, Heiges, M, Innamorato, F, Iodice, J, Kissinger, JC, Kraemer, E, Li, W, Miller, JA, Nayak, V, Pennington, C, Pinney, DF, Roos, DS, Ross, C, Stoeckert, CJ Jr, Treatman, C and Wang, H (2008) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acid Research 37, D539–D543.Google Scholar
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) Malavi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.CrossRefGoogle ScholarPubMed
Bensch, S, Canbäck, B, DeBarry, JD, Johansson, T, Hellgren, O, Kissinger, JC, Palinauskas, V, Videvall, E and Valkiūnas, G (2016) The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biology and Evolution 8, 1361–1373.Google Scholar
Boehme, U, Otto, TD, Cotton, J, Steinbiss, S, Sanders, M, Oyola, SM, Nicot, A, Gandon, S, Patra, KP, Herd, C, Bushell, E, Modrzynska, KK, Billker, O, Vinetz, JM, Rivero, A, Newbold, CI and Berriman, M (2016) Complete avian malaria parasite genomes reveal host-specific parasite evolution in birds and mammals. bioRxiv. https://doi.org/101.101/086504.Google Scholar
Borner, J, Pick, C, Thiede, J and Kolawole, OM (2016) Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Molecular Phylogenetics and Evolution 94, 221–231.Google Scholar
Chan, XWA, Wrenger, C, Stahl, K, Bergmann, B, Winterberg, M, Müller, IB and Saliba, KJ (2013) Chemical and genetic validation of thiamine utilization as an antimalarial drug target. Nature Communications 4, 2060.Google Scholar
Cox, FE (2010) History of the discovery of the malaria parasites and their vectors. Parasites & Vectors 3, 5.Google Scholar
Frech, C and Chen, N (2011) Genome comparison of human and non-human malaria parasites reveals species subset-specific genes potentially linked to human disease. PLoS Computational Biology 7, e1002320.Google Scholar
Helliwell, KE, Wheeler, GL and Smith, AG (2013) Widespread decay of vitamin-related pathways: coincidence or consequence? Trends in Genetics 29, 469–478.Google Scholar
Kemen, E, Gardiner, A, Schultz-Larsen, T, Kemen, AC, Balmuth, AL, Robert-Seilaniantz, A, Bailey, K, Holub, E, Studholme, DJ, MacLean, D and Jones, JDG (2011) Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biology 9, e1001094.Google Scholar
Kissinger, JC and DeBarry, J (2011) Genome cartography: charting the apicomplexan genome. Trends in Parasitology 27, 345–354.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Lee, M.-C and Marx, CJ (2012) Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genetics 8, e1002651.CrossRefGoogle ScholarPubMed
Logan-Klumpler, FJ, De SIlva, N, Boehme, U, Rogers, MB, Vilarde, G, McQuillan, JA, Carver, T, Aslett, M, Olsen, C, Phan, SSI, Farris, C, Mitra, S, Ramasamy, G, Wang, H, Tivey, A, Jackson, A, Houston, R, Parkhill, J, Holden, M, Harb, OS, Brunk, BP, Myler, PJ, Roos, D, Carrington, M, Smith, DF, Hertz-Fowler, C and Berriman, M (2012) GeneDB-an annotation database for pathogens. Nucleic Acid Research 40, D98–D108. https://doi.org/10.1093/nar/gkr1032.CrossRefGoogle ScholarPubMed
Martinsen, ES, Perkins, SL and Schall, JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.Google Scholar
McGhee, RB, Singh, SD and Weathersby, AB (1977) Plasmodium gallinaceum: vaccination in chickens. Experimental Parasitology 43, 231–238.CrossRefGoogle ScholarPubMed
Müller, S and Kappes, B (2007) Vitamin and cofactor biosynthesis pathways in Plasmodium and other apicomplexan parasites. Trends in Parasitology 23, 112–121.Google Scholar
Perkins, SL (2014) Malaria's many mates: past, present, and future of the systematics of the order Haemosporida. The Journal of Parasitology 100, 11–25.Google Scholar
Pick, C, Ebersberger, I, Spielmann, T, Bruchhaus, I and Burmester, T (2011) Phylogenomic analyses of malaria parasites and evolution of their exported proteins. BMC Evolutionary Biology 11, 167.Google Scholar
Pombert, J.-F, Selman, M, Burki, F, Bardell, FT, Farinelli, L, Solter, LF, Whitman, DW, Weiss, LM, Corradi, N and Keeling, PJ (2012) Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proceedings of the National Academy of Sciences of the USA 109, 12638–12643.Google Scholar
Sakharkar, KR, Sakharkar, MK and Chow, VTK (2007) Gene loss and gene conservation in obligatory intracellular parasites of human. Current Bioinformatics 2, 214–221.Google Scholar
Schaer, J, Perkins, SL, Decher, J, Leendertz, FH, Fahr, J, Weber, N and Matuschewski, K (2013) High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proceedings of the National Academy of Sciences 110, 17415–17419.Google Scholar
Shanmugasundram, A, Gonzalez-Galarza, FF, Wastling, JM, Vasieva, O and Jones, AR (2013) Library of apicomplexan metabolic pathways: a manually curated database for metabolic pathways of apicomplexan parasites. Nucleic Acids Research 41, D706–D713.Google Scholar
Tamas, I, Klasson, LM, Sandstrom, JP and Andersson, S (2001) Mutualists and parasites: how to paint yourself into a (metabolic) corner. Febs Letters 498, 135–139.CrossRefGoogle ScholarPubMed
Valkiunas, G (ed.) (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, Florida: CRC.Google Scholar
Videvall, E, Cornwallis, CK, Palinauskas, V, Valkiūnas, G and Hellgren, O (2015) The avian transcriptome response to malaria infection. Molecular Biology and Evolution 32, 1255–1267.Google Scholar
Videvall, E, Cornwallis, CK, Ahren, D, Palinauskas, V, Valkiūnas, G and Hellgren, O (2017) The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host-specific gene expression. Molecular Ecology 26, 2939–2958.Google Scholar
von Wasielewski, TKWN (1904–08) Studien und Mikrophotogramme zur Kenntnis der pathogenen Protozoen. Leipzig: Barth.CrossRefGoogle Scholar
Weatherby, K and Carter, D (2013) Chromera velia: the missing link in the evolution of parasitism. Advances in Applied Microbiology 85, 119–144.Google Scholar
Wrenger, C, Eschbach, M-L, Müller, IB, Laun, NP, Begley, TP and Walter, RD (2006) Vitamin B1 de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine. Biological Chemistry 387, 41–51.CrossRefGoogle ScholarPubMed
Supplementary material: File

Hellgren et al supplementary material 1

Supplementary Figure

Download Hellgren et al supplementary material 1(File)
File 10.7 MB