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Article

Domain Truncation in Hispidin Synthase Orthologs from Non-Bioluminescent Fungi Does Not Lead to Hispidin Biosynthesis

by
Kseniia A. Palkina
1,2,
Anastasia V. Balakireva
1,2,
Olga A. Belozerova
1,3,
Tatiana V. Chepurnykh
1,
Nadezhda M. Markina
1,2,
Sergey I. Kovalchuk
1,
Aleksandra S. Tsarkova
1,3,
Alexander S. Mishin
1,2,
Ilia V. Yampolsky
1,3 and
Karen S. Sarkisyan
1,2,4,5,*
1
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, Russia
2
Planta LLC., 121205 Moscow, Russia
3
Institute of Translational Medicine, Pirogov Russian National Research Medical University, 117997 Moscow, Russia
4
Synthetic Biology Group, MRC London Institute of Medical Sciences, London W12 0NN, UK
5
Institute of Clinical Sciences, Faculty of Medicine and Imperial College Centre for Synthetic Biology, Imperial College London, London SW7 2AZ, UK
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2023, 24(2), 1317; https://doi.org/10.3390/ijms24021317
Submission received: 13 November 2022 / Revised: 22 December 2022 / Accepted: 7 January 2023 / Published: 10 January 2023
(This article belongs to the Special Issue Advanced Research in Fluorescent Proteins)
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Abstract

Hispidin is a polyketide found in plants and fungi. In bioluminescent fungi, hispidin serves as a precursor of luciferin and is produced by hispidin synthases. Previous studies revealed that hispidin synthases differ in orthologous polyketide synthases from non-bioluminescent fungi by the absence of two domains with predicted ketoreductase and dehydratase activities. Here, we investigated the hypothesis that the loss of these domains in evolution led to the production of hispidin and the emergence of bioluminescence. We cloned three orthologous polyketide synthases from non-bioluminescent fungi, as well as their truncated variants, and assessed their ability to produce hispidin in a bioluminescence assay in yeast. Interestingly, expression of the full-length enzyme hsPKS resulted in dim luminescence, indicating that small amounts of hispidin are likely being produced as side products of the main reaction. Deletion of the ketoreductase and dehydratase domains resulted in no luminescence. Thus, domain truncation by itself does not appear to be a sufficient step for the emergence of efficient hispidin synthases from orthologous polyketide synthases. At the same time, the production of small amounts of hispidin or related compounds by full-length enzymes suggests that ancestral fungal species were well-positioned for the evolution of bioluminescence.
Keywords: bioluminescence; fungi; hispidin; α-pyrones; polyketide synthases; caffeic acid bioluminescence; fungi; hispidin; α-pyrones; polyketide synthases; caffeic acid

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MDPI and ACS Style

Palkina, K.A.; Balakireva, A.V.; Belozerova, O.A.; Chepurnykh, T.V.; Markina, N.M.; Kovalchuk, S.I.; Tsarkova, A.S.; Mishin, A.S.; Yampolsky, I.V.; Sarkisyan, K.S. Domain Truncation in Hispidin Synthase Orthologs from Non-Bioluminescent Fungi Does Not Lead to Hispidin Biosynthesis. Int. J. Mol. Sci. 2023, 24, 1317. https://doi.org/10.3390/ijms24021317

AMA Style

Palkina KA, Balakireva AV, Belozerova OA, Chepurnykh TV, Markina NM, Kovalchuk SI, Tsarkova AS, Mishin AS, Yampolsky IV, Sarkisyan KS. Domain Truncation in Hispidin Synthase Orthologs from Non-Bioluminescent Fungi Does Not Lead to Hispidin Biosynthesis. International Journal of Molecular Sciences. 2023; 24(2):1317. https://doi.org/10.3390/ijms24021317

Chicago/Turabian Style

Palkina, Kseniia A., Anastasia V. Balakireva, Olga A. Belozerova, Tatiana V. Chepurnykh, Nadezhda M. Markina, Sergey I. Kovalchuk, Aleksandra S. Tsarkova, Alexander S. Mishin, Ilia V. Yampolsky, and Karen S. Sarkisyan. 2023. "Domain Truncation in Hispidin Synthase Orthologs from Non-Bioluminescent Fungi Does Not Lead to Hispidin Biosynthesis" International Journal of Molecular Sciences 24, no. 2: 1317. https://doi.org/10.3390/ijms24021317

APA Style

Palkina, K. A., Balakireva, A. V., Belozerova, O. A., Chepurnykh, T. V., Markina, N. M., Kovalchuk, S. I., Tsarkova, A. S., Mishin, A. S., Yampolsky, I. V., & Sarkisyan, K. S. (2023). Domain Truncation in Hispidin Synthase Orthologs from Non-Bioluminescent Fungi Does Not Lead to Hispidin Biosynthesis. International Journal of Molecular Sciences, 24(2), 1317. https://doi.org/10.3390/ijms24021317

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