Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated trichomonas vaginalis genome

Lenka Horváthová, Lucie Šafaříková, Marek Basler, Ivan Hrdý, Neritza B. Campo, Jhy-Wei Shin, Kuo Yang Huang, Po Jung Huang, Rose Lin, Petrus Tang, Jan Tachezy

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Gene duplication is an important evolutionary mechanism and no eukaryote has more duplicated gene families than the parasitic protist Trichomonas vaginalis. Iron is an essential nutrient for Trichomonas and plays a pivotal role in the establishment of infection, proliferation, and virulence. To gain insight into the role of iron in T. vaginalis gene expression and genome evolution, we screened iron-regulated genes using an oligonucleotide microarray for T. vaginalis and by comparative EST (expressed sequence tag) sequencing of cDNA libraries derived from trichomonads cultivated under iron-rich (+Fe) and iron-restricted (-Fe) conditions. Among 19,000 ESTs from both libraries, we identified 336 iron-regulated genes, of which 165 were upregulated under +Fe conditions and 171 under -Fe conditions. The microarray analysis revealed that 195 of 4,950 unique genes were differentially expressed. Of these, 117 genes were upregulated under +Fe conditions and 78 were upregulated under -Fe conditions. The results of both methods were congruent concerning the regulatory trends and the representation of gene categories. Under +Fe conditions, the expression of proteins involved in carbohydrate metabolism, particularly in the energy metabolism of hydrogenosomes, and in methionine catabolism was increased. The iron-sulfur cluster assembly machinery and certain cysteine proteases are of particular importance among the proteins upregulated under -Fe conditions. A unique feature of the T. vaginalis genome is the retention during evolution of multiple paralogous copies for a majority of all genes. Although the origins and reasons for this gene expansion remain unclear, the retention of multiple gene copies could provide an opportunity to evolve differential expression during growth in variable environmental conditions. For genes whose expression was affected by iron, we found that iron influenced the expression of only some of the paralogous copies, whereas the expression of the other paralogs was iron independent. This finding indicates a very stringent regulation of the differentially expressed paralogous genes in response to changes in the availability of exogenous nutrients and provides insight into the evolutionary rationale underlying massive paralog retention in the Trichomonas genome.

Original languageEnglish
Pages (from-to)1017-1029
Number of pages13
JournalGenome Biology and Evolution
Volume4
Issue number10
DOIs
Publication statusPublished - 2012 Dec 1

Fingerprint

Trichomonas vaginalis
transcriptomics
Iron
genome
Genome
iron
gene
Genes
genes
Trichomonas
Expressed Sequence Tags
gene expression
Trichomonadida
metabolism
Gene Expression
Food
Gene Duplication
Cysteine Proteases
cysteine proteinases
Carbohydrate Metabolism

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Horváthová, Lenka ; Šafaříková, Lucie ; Basler, Marek ; Hrdý, Ivan ; Campo, Neritza B. ; Shin, Jhy-Wei ; Huang, Kuo Yang ; Huang, Po Jung ; Lin, Rose ; Tang, Petrus ; Tachezy, Jan. / Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated trichomonas vaginalis genome. In: Genome Biology and Evolution. 2012 ; Vol. 4, No. 10. pp. 1017-1029.
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abstract = "Gene duplication is an important evolutionary mechanism and no eukaryote has more duplicated gene families than the parasitic protist Trichomonas vaginalis. Iron is an essential nutrient for Trichomonas and plays a pivotal role in the establishment of infection, proliferation, and virulence. To gain insight into the role of iron in T. vaginalis gene expression and genome evolution, we screened iron-regulated genes using an oligonucleotide microarray for T. vaginalis and by comparative EST (expressed sequence tag) sequencing of cDNA libraries derived from trichomonads cultivated under iron-rich (+Fe) and iron-restricted (-Fe) conditions. Among 19,000 ESTs from both libraries, we identified 336 iron-regulated genes, of which 165 were upregulated under +Fe conditions and 171 under -Fe conditions. The microarray analysis revealed that 195 of 4,950 unique genes were differentially expressed. Of these, 117 genes were upregulated under +Fe conditions and 78 were upregulated under -Fe conditions. The results of both methods were congruent concerning the regulatory trends and the representation of gene categories. Under +Fe conditions, the expression of proteins involved in carbohydrate metabolism, particularly in the energy metabolism of hydrogenosomes, and in methionine catabolism was increased. The iron-sulfur cluster assembly machinery and certain cysteine proteases are of particular importance among the proteins upregulated under -Fe conditions. A unique feature of the T. vaginalis genome is the retention during evolution of multiple paralogous copies for a majority of all genes. Although the origins and reasons for this gene expansion remain unclear, the retention of multiple gene copies could provide an opportunity to evolve differential expression during growth in variable environmental conditions. For genes whose expression was affected by iron, we found that iron influenced the expression of only some of the paralogous copies, whereas the expression of the other paralogs was iron independent. This finding indicates a very stringent regulation of the differentially expressed paralogous genes in response to changes in the availability of exogenous nutrients and provides insight into the evolutionary rationale underlying massive paralog retention in the Trichomonas genome.",
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Horváthová, L, Šafaříková, L, Basler, M, Hrdý, I, Campo, NB, Shin, J-W, Huang, KY, Huang, PJ, Lin, R, Tang, P & Tachezy, J 2012, 'Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated trichomonas vaginalis genome', Genome Biology and Evolution, vol. 4, no. 10, pp. 1017-1029. https://doi.org/10.1093/gbe/evs078

Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated trichomonas vaginalis genome. / Horváthová, Lenka; Šafaříková, Lucie; Basler, Marek; Hrdý, Ivan; Campo, Neritza B.; Shin, Jhy-Wei; Huang, Kuo Yang; Huang, Po Jung; Lin, Rose; Tang, Petrus; Tachezy, Jan.

In: Genome Biology and Evolution, Vol. 4, No. 10, 01.12.2012, p. 1017-1029.

Research output: Contribution to journalArticle

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T1 - Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated trichomonas vaginalis genome

AU - Horváthová, Lenka

AU - Šafaříková, Lucie

AU - Basler, Marek

AU - Hrdý, Ivan

AU - Campo, Neritza B.

AU - Shin, Jhy-Wei

AU - Huang, Kuo Yang

AU - Huang, Po Jung

AU - Lin, Rose

AU - Tang, Petrus

AU - Tachezy, Jan

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