The regulatory mechanism underlying light-inducible production of carotenoids in nonphototrophic bacteriaFootnote

This review was written in response to the author’s receipt of the JSBBA Award for Young Scientists in 2015.

References

• Herrou J, Crosson S. Function, structure and mechanism of bacterial photosensory LOV proteins. Nat. Rev. Microbiol. 2011;9:713–723.10.1038/nrmicro2622
   PubMed Web of Science ®Google Scholar
• Purcell EB, Crosson S. Photoregulation in prokaryotes. Curr. Opin. Microbiol. 2008;11:168–178.10.1016/j.mib.2008.02.014
   PubMed Web of Science ®Google Scholar
• Van der Horst MA, Hellingwerf KJ. Photoreceptor proteins, “star actors of modern times”:  a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc. Chem. Res. 2004;37:13–20.10.1021/ar020219d
   PubMed Web of Science ®Google Scholar
• Falciatore A, Bowler C. The evolution and function of blue and red light photoreceptors. Curr. Top. Dev. Biol. 2005;68:317–350.
   PubMed Web of Science ®Google Scholar
• Herrera-Estrella A, Horwitz BA. Looking through the eyes of fungi: molecular genetics of photoreception. Mol. Microbiol. 2007;64:5–15.10.1111/mmi.2007.64.issue-1
   PubMed Web of Science ®Google Scholar
• Nisar N, Li L, Lu S, et al. Carotenoid metabolism in plants. Mol. Plant. 2015;8:68–82.10.1016/j.molp.2014.12.007
   PubMed Web of Science ®Google Scholar
• Avalos J. Biological roles of fungal carotenoids. Curr. Genet. 2015;61:309–324.10.1007/s00294-014-0454-x
   PubMed Web of Science ®Google Scholar
• Takaichi S. Carotenoids in algae: distributions, biosyntheses and functions. Mar. Drugs. 2011;9:1101–1118.10.3390/md9061101
   PubMed Web of Science ®Google Scholar
• Vachali P, Bhosale P, Bernstein PS. Microbial carotenoids. Methods Mol. Biol. 2012;898:41–59.10.1007/978-1-61779-918-1
   PubMedGoogle Scholar
• Edge R, McGarvey DJ, Truscott TG. The carotenoids as anti-oxidants–a review. J. Photochem. Photobiol. B. 1997;41:189–200.10.1016/S1011-1344(97)00092-4
   PubMed Web of Science ®Google Scholar
• Takano H, Asker D, Beppu T, et al. Genetic control for light-induced carotenoid production in non-phototrophic bacteria. J. Ind. Microbiol. Biotechnol. 2006;33:88–93.10.1007/s10295-005-0005-z
   PubMed Web of Science ®Google Scholar
• Koyama Y, Kato F, Yazawa Y. Effect of light on the pigmentation of bacteria in Actinomycetales. In: Arai T, editor. Actinomycetales, the boundary microorganisms. Tokyo: Toppan; 1976. p. 65–85.
   Google Scholar
• Netzer R, Stafsnes MH, Andreassen T, et al. Biosynthetic pathway for γ-cyclic sarcinaxanthin in Micrococcus luteus: heterologous expression and evidence for diverse and multiple catalytic functions of C(50) carotenoid cyclases. J. Bacteriol. 2010;192:5688–5699.10.1128/JB.00724-10
   PubMed Web of Science ®Google Scholar
• Lee HS, Ohnishi Y, Horinouchi S. A sigmaB-like factor responsible for carotenoid biosynthesis in Streptomyces griseus. J. Mol. Microbiol. Biotechnol. 2001;3:95–101.
   PubMed Web of Science ®Google Scholar
• Kato F, Hino T, Nakaji A, et al. Carotenoid synthesis in Streptomyces setonii ISP5395 is induced by the gene crtS, whose product is similar to a sigma factor. Mol. Gen. Genet. 1995;247:387–390.10.1007/BF00293207
   PubMedGoogle Scholar
• Ramakrishnan L, Tran H, Federspiel N, et al. A crtB homolog essential for photochromogenicity in Mycobacterium marinum: isolation, characterization, and gene disruption via homologous recombination. J. Bacteriol. 1997;179:5862–5868.
   PubMed Web of Science ®Google Scholar
• Gao L, Groger R, Cox J, et al. Transposon mutagenesis of Mycobacterium marinum identifies a locus linking pigmentation and intracellular survival. Infect. Immun. 2003;71:922–929.10.1128/IAI.71.2.922-929.2003
   PubMed Web of Science ®Google Scholar
• López-Rubio JJ, Padmanabhan S, Lázaro JM, et al. Operator design and mechanism for CarA repressor-mediated down-regulation of the photoinducible CarB operon in Myxococcus xanthus. J. Biol. Chem. 2004;279:28945–28953.10.1074/jbc.M403459200
   PubMed Web of Science ®Google Scholar
• Pérez-Marín MC, López-Rubio JJ, Murillo FJ, et al. The N terminus of Myxococcus xanthus CarA repressor is an autonomously folding domain that mediates physical and functional interactions with both operator dna and antirepressor protein. J. Biol. Chem. 2004;279:33093–33103.10.1074/jbc.M405225200
   PubMed Web of Science ®Google Scholar
• León E, Navarro-Avilés G, Santiveri CM, et al. A bacterial antirepressor with SH3 domain topology mimics operator DNA in sequestering the repressor DNA recognition helix. Nucleic Acids Res. 2010;38:5226–5241.10.1093/nar/gkq277
   PubMed Web of Science ®Google Scholar
• Whitworth DE, Bryan SJ, Berry AE, et al. Genetic dissection of the light-inducible carqrs promoter region of Myxococcus xanthus. J. Bacteriol. 2004;186:7836–7846.10.1128/JB.186.23.7836-7846.2004
   PubMed Web of Science ®Google Scholar
• Browning DF, Whitworth DE, Hodgson DA. Light-induced carotenogenesis in Myxococcus xanthus: functional characterization of the ECF sigma factor CarQ and antisigma factor CarR. Mol. Microbiol. 2003;48:237–251.10.1046/j.1365-2958.2003.03431.x
   PubMed Web of Science ®Google Scholar
• Gorham HC, McGowan SJ, Robson PR, et al. Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol. Microbiol. 1996;19:171–186.10.1046/j.1365-2958.1996.360888.x
   PubMed Web of Science ®Google Scholar
• Chandra G, Chater KF. Developmental biology of Streptomyces from the perspective of 100 actinobacterial genome sequences. FEMS Microbiol. Rev. 2013;38:345–379.
   PubMed Web of Science ®Google Scholar
• Liu G, Chater KF, Chandra G, et al. Molecular regulation of antibiotic biosynthesis in streptomyces. Microbiol. Mol. Biol. Rev. 2013;77:112–143.10.1128/MMBR.00054-12
   PubMed Web of Science ®Google Scholar
• Houssaini-Iraqui M, Lazraq MH, Clavel-Sérès S, et al. Cloning and expression of Mycobacterium aurum carotenogenesis genes in Mycobacterium smegmatis. FEMS Microbiol. Lett. 1992;90:239–244.10.1111/fml.1992.90.issue-3
   Web of Science ®Google Scholar
• Krügel H, Krubasik P, Weber K, et al. Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim. Biophys. Acta. 1999;1439:57–64.10.1016/S1388-1981(99)00075-X
   PubMed Web of Science ®Google Scholar
• Bentley SD, Chater KF, Cerdeno-Tarraga AM, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature. 2002;417:141–147.10.1038/417141a
   PubMed Web of Science ®Google Scholar
• Takano H, Obitsu S, Beppu T, et al. Light-induced carotenogenesis in Streptomyces coelicolor a3(2): identification of an extracytoplasmic function sigma factor that directs photodependent transcription of the carotenoid biosynthesis gene cluster. J. Bacteriol. 2005;187:1825–1832.10.1128/JB.187.5.1825-1832.2005
   PubMed Web of Science ®Google Scholar
• Brown NL, Stoyanov JV, Kidd SP, et al. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 2003;27:145–163.10.1016/S0168-6445(03)00051-2
   PubMed Web of Science ®Google Scholar
• Hobman JL. MerR family transcription activators: similar designs, different specificities. Mol. Microbiol. 2007;63:1275–1278.10.1111/mmi.2007.63.issue-5
   PubMed Web of Science ®Google Scholar
• Takano H, Beppu T, Ueda K. The CarA/LitR-family transcriptional regulator: Its possible role as a photosensor and wide distribution in non-phototrophic bacteria. Biosci. Biotechnol. Biochem. 2006;70:2320–2324.10.1271/bbb.60230
   PubMed Web of Science ®Google Scholar
• Takano H, Hagiwara K, Ueda K. Fundamental role of cobalamin biosynthesis in the developmental growth of Streptomyces coelicolor A3 (2). Appl. Microbiol. Biotechnol. 2015;99:2329–2337.10.1007/s00253-014-6325-z
   PubMed Web of Science ®Google Scholar
• Takano H, Nishiyama T, Amano SI, et al. Streptomyces metabolites in divergent microbial interactions. J. Ind. Microbiol. Biotechnol. 2016;43:143–148.10.1007/s10295-015-1680-z
   PubMed Web of Science ®Google Scholar
• Medema MH, Fischbach MA. Computational approaches to natural product discovery. Nat. Chem. Biol. 2015;11:639–648.10.1038/nchembio.1884
   PubMed Web of Science ®Google Scholar
• Teh BS, Lau NS, Ng FL, et al. Complete genome sequence of the thermophilic Thermus sp. CCB_US3_UF1 from a hot spring in Malaysia. Stand. Genomic Sci. 2015;10:289.10.1186/s40793-015-0053-6
   Web of Science ®Google Scholar
• Jentzsch K, Wirtz A, Circolone F, et al. Mutual exchange of kinetic properties by extended mutagenesis in two short LOV domain proteins from Pseudomonas putida. Biochemistry. 2009;48:10321–10333.10.1021/bi901115z
   PubMed Web of Science ®Google Scholar
• Bamann C, Bamberg E, Wachtveitl J, et al. Proteorhodopsin. Biochim. Biophys. Acta. 1837;2014:614–625.
   Google Scholar
• Brown LS. Eubacterial rhodopsins — unique photosensors and diverse ion pumps. Biochim. Biophys. Acta. 2014;1837:553–561.10.1016/j.bbabio.2013.05.006
   PubMed Web of Science ®Google Scholar
• Land M, Lapidus A, Mayilraj S, et al. Complete genome sequence of Actinosynnema mirum type strain (101T). Stand. Genomic Sci. 2009;1:46–53.10.4056/sigs.21137
   PubMed Web of Science ®Google Scholar
• Ichikawa N, Oguchi A, Ikeda H, et al. Genome sequence of Kitasatospora setae nbrc 14216t: an evolutionary snapshot of the family Streptomycetaceae. DNA Res. 2010;17:393–406.10.1093/dnares/dsq026
   PubMed Web of Science ®Google Scholar
• Zhao W, Zhong Y, Yuan H, et al. Complete genome sequence of the rifamycin SV-producing Amycolatopsis mediterranei U32 revealed its genetic characteristics in phylogeny and metabolism. Cell Res. 2010;20:1096–1108.10.1038/cr.2010.87
   PubMed Web of Science ®Google Scholar
• Henne A, Brüggemann H, Raasch C, et al. The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 2004;22:547–553.10.1038/nbt956
   PubMed Web of Science ®Google Scholar
• Brüggemann H, Chen C. Comparative genomics of Thermus thermophilus: plasticity of the megaplasmid and its contribution to a thermophilic lifestyle. J. Biotechnol. 2006;124:654–661.10.1016/j.jbiotec.2006.03.043
   PubMed Web of Science ®Google Scholar
• Eppinger M, Bunk B, Johns MA, et al. Genome sequences of the biotechnologically important Bacillus megaterium strains QM B1551 and DSM319. J. Bacteriol. 2011;193:4199–4213.10.1128/JB.00449-11
   PubMed Web of Science ®Google Scholar
• Bunk B, Schulz A, Stammen S, et al. A short story about a big magic bug. Bioeng Bugs. 2010;1:85–91.10.4161/bbug.1.2.11101
   PubMedGoogle Scholar
• Takano H, Kondo M, Usui N, et al. Involvement of CarA/LitR and CRP/FNR family transcriptional regulators in light-induced carotenoid production in Thermus thermophilus. J. Bacteriol. 2011;193:2451–2459.10.1128/JB.01125-10
   PubMed Web of Science ®Google Scholar
• Green J, Scott C, Guest JR. Functional versatility in the CRP-FNR superfamily of transcription factors: FNR and FLP. Adv. Microb. Physiol. 2001;44:1–34.10.1016/S0065-2911(01)44010-0
   PubMed Web of Science ®Google Scholar
• Yokoyama A, Shizuri Y, Hoshino T, et al. Thermocryptoxanthins: novel intermediates in the carotenoid biosynthetic pathway of Thermus thermophilus. Arch. Microbiol. 1996;165:342–345.10.1007/s002030050336
   PubMed Web of Science ®Google Scholar
• Agari Y, Kuramitsu S, Shinkai A. X-ray crystal structure of TTHB099, a CRP/FNR superfamily transcriptional regulator from Thermus thermophilus HB8, reveals a DNA-binding protein with no required allosteric effector molecule. Proteins. 2012;80:1490–1494.10.1002/prot.24049
   PubMed Web of Science ®Google Scholar
• Popovych N, Tzeng SR, Tonelli M, et al. Structural basis for cAMP-mediated allosteric control of the catabolite activator protein. Proc. Natl. Acad. Sci. USA. 2009;106:6927–6932.10.1073/pnas.0900595106
   PubMed Web of Science ®Google Scholar
• Ortiz-Guerrero JM, Polanco MC, Murillo FJ, et al. Light-dependent gene regulation by a coenzyme B12-based photoreceptor. Proc. Natl. Acad. Sci. USA. 2011;108:7565–7570.10.1073/pnas.1018972108
   PubMed Web of Science ®Google Scholar
• Díez AI, Ortiz-Guerrero JM, Ortega A, et al. Analytical ultracentrifugation studies of oligomerization and DNA-binding of TtCarH, a Thermus thermophilus coenzyme B12-based photosensory regulator. Eur. Biophys. J. 2013;42:463–476.10.1007/s00249-013-0897-x
   PubMed Web of Science ®Google Scholar
• Mondol MA, Shin HJ, Islam MT. Diversity of secondary metabolites from marine bacillus species: chemistry and biological activity. Mar. Drugs. 2013;11:2846–2872.10.3390/md11082846
   PubMed Web of Science ®Google Scholar
• Maeda I. Genetic modification in Bacillus subtilis for production of C30 carotenoids. Methods Mol. Biol. 2012;892:197–205.10.1007/978-1-61779-879-5
   PubMedGoogle Scholar
• Steiger S, Perez-Fons L, Fraser PD, et al. Biosynthesis of a novel C30 carotenoid in Bacillus firmus isolates. J. Appl. Microbiol. 2012;113:888–895.10.1111/jam.2012.113.issue-4
   PubMed Web of Science ®Google Scholar
• Khaneja R, Perez-Fons L, Fakhry S, et al. Carotenoids found in Bacillus. J. Appl .Microbiol. 2010;108:1889–1902.
   PubMed Web of Science ®Google Scholar
• Takano H, Mise K, Hagiwara K, et al. Role and function of LitR, an Adenosyl B 12 -bound light-sensitive regulator of bacillus megaterium QM b1551, in regulation of carotenoid production. J. Bacteriol. 2015;197:2301–2315.10.1128/JB.02528-14
   PubMed Web of Science ®Google Scholar
• Takano H, Agari Y, Hagiwara K, et al. LdrP, a cAMP receptor protein/FNR family transcriptional regulator, serves as a positive regulator for the light-inducible gene cluster in the megaplasmid of Thermus thermophilus. Microbiology. 2014;160:2650–2660.10.1099/mic.0.082263-0
   PubMed Web of Science ®Google Scholar
• Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011;28:2731–2739.10.1093/molbev/msr121
   PubMed Web of Science ®Google Scholar