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Proc Natl Acad Sci U S A. 2018 Dec 11;115(50):12728-12732. doi: 10.1073/pnas.1803615115. Epub 2018 Nov 26.

Genetically encodable bioluminescent system from fungi.

Author information

1
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, Russia.
2
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, Russia; karen@planta.bio ivyamp@gmail.com.
3
Planta LLC, 121205 Moscow, Russia.
4
Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.
5
Medical Research Council London Institute of Medical Sciences, Imperial College London, W12 0NN London, United Kingdom.
6
Centre for Genomic Regulation, The Barcelona Institute for Science and Technology, 08003 Barcelona, Spain.
7
Universitat Pompeu Fabra, 08003 Barcelona, Spain.
8
Evrogen JSC, 117997 Moscow, Russia.
9
Institute of Biophysics, Federal Research Center Krasnoyarsk Science Center, Siberian Branch, Russian Academy of Sciences, 660036 Krasnoyarsk, Russia.
10
Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, 142290 Moscow, Russia.
11
Pirogov Russian National Research Medical University, 117997 Moscow, Russia.
12
Biomedical Nanomaterials, National Research Technological University (MISiS), 119049 Moscow, Russia.
13
Skolkovo Institute of Science and Technology, 121205 Moscow, Russia.
14
Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, 05508-000 São Paulo, Brazil.
15
Departamento de Oceanografia Física, Química e Geológica, Instituto Oceanográfico, Universidade de São Paulo, 05508-120 São Paulo, Brazil.
16
Department of Environmental Biology, Chubu University, 487-8501 Kasugai, Japan.
17
Catalan Institution for Research and Advanced Studies (ICREA), 08010 Barcelona, Spain.
18
Departamento de Química Fundamental, Instituto de Química, Universidade de São Paulo, 05508-000 São Paulo, Brazil.

Abstract

Bioluminescence is found across the entire tree of life, conferring a spectacular set of visually oriented functions from attracting mates to scaring off predators. Half a dozen different luciferins, molecules that emit light when enzymatically oxidized, are known. However, just one biochemical pathway for luciferin biosynthesis has been described in full, which is found only in bacteria. Here, we report identification of the fungal luciferase and three other key enzymes that together form the biosynthetic cycle of the fungal luciferin from caffeic acid, a simple and widespread metabolite. Introduction of the identified genes into the genome of the yeast Pichia pastoris along with caffeic acid biosynthesis genes resulted in a strain that is autoluminescent in standard media. We analyzed evolution of the enzymes of the luciferin biosynthesis cycle and found that fungal bioluminescence emerged through a series of events that included two independent gene duplications. The retention of the duplicated enzymes of the luciferin pathway in nonluminescent fungi shows that the gene duplication was followed by functional sequence divergence of enzymes of at least one gene in the biosynthetic pathway and suggests that the evolution of fungal bioluminescence proceeded through several closely related stepping stone nonluminescent biochemical reactions with adaptive roles. The availability of a complete eukaryotic luciferin biosynthesis pathway provides several applications in biomedicine and bioengineering.

KEYWORDS:

bioluminescence; fungal luciferase; fungal luciferin biosynthesis

PMID:
30478037
PMCID:
PMC6294908
DOI:
10.1073/pnas.1803615115
[Indexed for MEDLINE]
Free PMC Article

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