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The Evolution of Histidine Biosynthesis in Archaea: Insights into the his Genes Structure and Organization in LUCA

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Abstract

The available sequences of genes encoding the enzymes associated with histidine biosynthesis suggest that this is an ancient metabolic pathway that was assembled prior to the diversification of Bacteria, Archaea, and Eucarya. Paralogous duplication, gene elongation, and fusion events of several different his genes have played a major role in shaping this biosynthetic route. We have analyzed the structure and organization of histidine biosynthetic genes from 55 complete archaeal genomes and combined it with phylogenetic inference in order to investigate the mechanisms responsible for the assembly of the his pathway and the origin of his operons. We show that a wide variety of different organizations of his genes exists in Archaea and that some his genes or entire his (sub-)operons have been likely transferred horizontally between Archaea and Bacteria. However, we show that, in most Archaea, his genes are monofunctional (except for hisD) and scattered throughout the genome, suggesting that his operons might have been assembled multiple times during evolution and that in some cases they are the result of recent evolutionary events. An evolutionary model for the structure and organization of his genes in LUCA is proposed.

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Abbreviations

HisG:

ATP phosphoribosyl transferase (EC 2.4.2.17)

HisD:

Histidinol dehydrogenase (EC 1.1.1.23)

HisC:

Histidinol-phosphate aminotransferase (EC 2.6.1.9)

HisN:

Histidinol-phosphate phosphatase (EC 3.1.3.15)

HisB:

Imidazoleglycerol-phosphate dehydratase (EC 4.2.1.19)

HisH:

G-type glutamine amidotransferase

HisA:

[N-(5_-phosphoribosyl) formimino]-5-aminoimidazole-4-carboxamide ribonucleotide isomerase (EC 5.3.1.16)

HisF:

Imidazole glycerol phosphate synthase subunit HisF (EC 4.1.3.-)

HisI:

Phosphoribosyl-AMP cyclohydrolase (EC 3.5.4.19)

HisE:

Phosphoribosyl-ATP pyrophosphatase (EC 3.6.1.31)

LUCA:

Last universal common ancestor

HGT:

Horizontal gene transfer

PRFAR:

N-(5′phospho-d-1′-ribulosylformimino)-5-amino-1-(5-phosphoribosyl)-4-imidazolecarboxamide

AICAR:

5-Aminoimidazole-4-carboxamide ribonucleoside

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Correspondence to Renato Fani.

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Fondi, M., Emiliani, G., Liò, P. et al. The Evolution of Histidine Biosynthesis in Archaea: Insights into the his Genes Structure and Organization in LUCA. J Mol Evol 69, 512–526 (2009). https://doi.org/10.1007/s00239-009-9286-6

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  • DOI: https://doi.org/10.1007/s00239-009-9286-6

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