The influence of light regulation on the growth and enzyme production of three endolichenic fungal isolates, i.e. Pseudopestalotiopsis theae (EF13), Fusarium solani (EF5), and Xylaria venustula (PH22), was determined. The isolates were exposed to blue, red, green, yellow, white fluorescent light (12 h light-12 h dark photoperiod) (test), and 24 h dark (control) conditions. Results revealed that the alternating light-dark conditions resulted in the formation of dark rings in most fungal isolates but was absent in PH22. Red light induced sporulation while yellow light elicited higher biomass in all isolates (0.19 ± 0.01 g, 0.07 ± 0.00 g, and 0.11 ± 0.00 g, for EF13, PH22, and EF5, respectively) as compared to incubation in the dark. Results also showed that blue light induced higher amylase activity in PH22 (15.31 ± 0.45 U/mL) and L-asparaginase activity in all isolates (0.45 ± 0.01 U/mL, 0.55 ± 0.39 U/mL, and 0.38 ± 0.01 U/mL, for EF13, PH22, and EF5, respectively) compared to both control conditions. Green light enhanced the production of xylanase (6.57 ± 0.42 U/mL, 10.64 ± 0.12 U/mL, and 7.55 ± 0.56 U/mL for EF13, PH22, and EF5, respectively) and cellulase (6.49 ± 0.48 U/mL, 9.57 ± 0.25 U/mL, and 7.28 ± 0.63 U/mL, for EF13, PH22, and EF5, respectively). In contrast, red light was the least effective light treatment as production of enzymes was the least, with lower levels of amylase, cellulase, xylanase, and L-asparaginase detected. To conclude, all three endolichenic fungi are light-responsive, with fungal growth regulated with the use of red light and yellow light, and manipulation of enzyme production via blue and green light.

School of Science Monash University Malaysia Jalan Lagoon Selatan Selangor Darul Ehsan 47500 Bandar Sunway Malaysia

Zobrazit více v PubMed

Abdel-Raou M, Aldeweik HM, Elbendary EY (2019) Impact of physical and chemical factors on L-asparaginase enzyme purified from soil bacteria. J Biol Sc 20:48–55 DOI

Adesina FC, Onilude AA (2013) Isolation, identification and screening of xylanase and glucanase-producing microfungi from degrading wood in Nigeria. Afr J Agric Res 8:4414–4421 DOI

Araujo NL, Avelino KV, Halabura MIW, Marim RA, Kassem ASS, Linde GA, Colauto NB, Doo-Valle JS (2021) Use of green light to improve the production of lignocellulose-decay enzymes by Pleurotus spp. in liquid cultivation. Enzyme Microb Technol 149:109860. https://doi.org/10.1016/j.enzmictec.2021.109860

Beier S, Hinterdobler W, Bazafkan H, Schillinger L, Schmoll M (2020) CLR1 and CLR2 are light dependent regulators of xylanase and pectinase genes in Trichoderma reesei. Fungal Genet Biol 136:103315.  https://doi.org/10.1016/j.fgb.2019.103315

Betina V, Zajacova J (1978) Regulation of periodicity and intensity of photo-induced conidiation of Trichoderma viride. Folia Microbiol 23:453–459 DOI

Bhattacharyya PN, Jha DK (2011) Optimization of cultural conditions affecting growth and improved bioactive metabolites production by a subsurface Aspergillus strain TSF 146. Int J Appl Biol Pharm 2:133–143

Bhunjun CS, Phillips AJL, Jayawardena RS, Promputtha I, Hyde KD (2021) Importance of molecular data to identify fungal plant pathogens and guidelines for pathogenicity testing based on Koch’s postulates. Pathogens 10:1096. https://doi.org/10.3390/pathogens10091096 PubMed DOI PMC

Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, Fischer R (2005) The Aspergillus nidulans phytochromes FphA represses sexual development in red light. Curr Biol 15:1833–1838 PubMed DOI

Brown LS (2004) Fungal rhodopsins and opsin-related proteins: eukaryotic homologues of bacteriorhodopsin with unknown functions. Photochem Photobiol Sci 3:555–565 PubMed DOI

Cai MH, Fang Z, Niu CP, Zhou XS, Zhang YX (2013) Light regulation on growth, development and secondary metabolism of marine-derived filamentous fungi. Folia Microbiol 58:537–546 DOI

Calvo AM, Wilson RA, Bok JW, Keller NP (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66:447–459 PubMed DOI PMC

Campbell MA, Medd RW, Brown JB (2003) Optimizing conditions for growth and sporulation of Pyrenophora semeniperda. Plant Pathol 52:448–454 DOI

Canessa P, Schumacher J, Hevia MA, Tudzynski P, Larrondo LF (2013) Assessing the effects of light on differentiation and virulence of the plant pathogen Botrytis cinerea: characterization of the white-collar complex. PLOS 8:e84223. https://doi.org/10.1371/journal.pone.0084223

Casas-Flores S, Rios-Momberg M, Rosales-Saavedra T, Martinez-Hernandez P, Olmedo-Monfil V, Herrera-Estrella A (2006) Cross-talk between a fungal blue light perception system and the cyclic AMP signalling pathway. Eukaryot Cell 5:499–506 PubMed DOI PMC

Cetz-Chel JE, Balcazar-Lopez D, Esquivel-Naranjo EU, Herrera-Estrella A (2016) The Trichoderma atroviride putative transcription factor Blu7 controls light responsiveness and tolerance. BMC Genom 17:e2016. https://doi.org/10.1186/s12864-016-2639-9

Chen HC, Dunlap JC, Loros JL (2010) Neurospora illuminates fungal photoreception. Fungal Genet Biol 47:922–929 PubMed DOI PMC

Cheng CW, Chen CK, Chang CJ, Chen LY (2012) Effect of colour LEDs on mycelia growth of Aspergillus ficuum and phytase production in photo-fermentations. J Photochem Photobiol B 106:81–86 PubMed DOI

Chow YY, Ting ASY (2015) Endophytic L-asparaginase-producing fungi from plants associated with anticancer properties. J Adv Res 56:869–876 DOI

Ding G, Li Y, Fu SB, Liu SC, Wei JC, Che YS (2009) Ambuic acid and torreyanic acid derivatives from the endolichenic fungus Pestalotiopsis sp. J Nat Prod 72:182–186 PubMed DOI

Elumalai P, Lim JM, Park YJ, Cho M, Shea PJ, Oh BT (2019) Enhanced amylase production by a Bacillus subtilis strain under blue light emitting diodes. Prep Biochem Biotech 49:143–150 DOI

Estrada AF, Avalos J (2009) Regulation and targeted mutation of opsA, coding for the nop-1 opsin orthologue in Fusarium fujukuroi. J Mol Biol 387:59–73 PubMed DOI

Farkas V, Nemcovic M (2001) Cell wall composition and polysaccharide synthase change following photoinduction in Trichoderma viride. Acta Bot Hung 52:281–288 DOI

Farris MH, Ford KA, Doyle RC (2016) Qualitative and quantitative assays for detection and characterization of protein antimicrobials. J Vis Exp 110:e53819. https://doi.org/10.3791/53819

Franco DL, Canessa P, Bellora N, Risau-Gusman S, Olivares-Yanes C, Perez-Lara R, Libkind D, Larrondo LF, Marpegan L (2017) Spontaneous circadian rhythms in a cold-adapted natural isolate of Aureobasidium pullalans. Sci Rep 7:13812–13837 DOI

Fuller KK, Loros JJ, Dunlap JC (2015) Fungal photobiology: visible light as a signal for stress, space and time. Curr Genet 61:275–288 PubMed DOI

Gan PT, Ting ASY (2019) Light mediation as a strategy to induce production of valuable microbial compounds. In: Microbial Technology for the Welfare of Society, Springer Singapore, Singapore, pp 101–123

Gyalai-Korpos M, Nagy G, Mareczky Z, Schuster A, Reczey K, Schmoll M (2010) Relevance of the light signalling machinery of cellulase expression in Trichoderma reesei (hypocrea jecorina). BMC Res Notes 3:330. https://doi.org/10.1186/1756-0500-3-330 PubMed DOI PMC

Ha SY, Jung JY, Park JH, Lee DH, Choi JW, Yang JK (2020) Effect of light-emitting diodes on cordycepin production in submerged Cordyceps militaris cultures. J Mushroom 18:10–19

Hill EP (1976) Effect of light on growth and sporulation of Aspergillus ornatus. J Gen Microbiol 95:39–44 PubMed DOI

Hosseinpour L, Zareei M, Boroujeni ZB, Yaghoubi R, Hashemi SJ (2017) Effect of different incubation temperatures, times, and colored lights on fungal biomass and black pigment (melanin) production in Exophiala crusticola. Infect Epidemiol Microbiol 3:90–95

Igbalajobi O, Yu ZZ, Fischer R (2019) Red and blue light sensing in the plant pathogen Alternaria alternata depends on phytochrome and the white collar protein LreA. Appl Environ Microbiol 10:e00371-e419. https://doi.org/10.1128/mBio.00371-19 DOI

Jain P, Gupta S (2012) Effect of carbon and nitrogen sources on antimicrobial metabolite production of endophytic fungus Penicillium sp. against human pathogen. J Pharm Res 5:4325–4328

Kannagara BTSDP, Rajapaksha RSCG, Paranagama PA (2009) Nature and bioactive of endolichenic fungi in Pseudocyphellaria sp, Parmotrema sp. and Usnea sp. at Hakgala montane forest in Sri Lanka. Lett Appl Microbiol 48:203–209 DOI

Keller NO, Nesbitt C, Sarr B, Phillips TD, Burow GB (1997) pH regulation of sterigmatocystin and aflatoxin biosynthesis in Aspergillus spp. Phytopathology 87:643–648 PubMed DOI

Kellogg JJ, Raja HA (2016) Endolichenic fungi: a new source of rich bioactive secondary metabolites on the horizon. Phytochem Rev 16:271–293 DOI

Kulkarni N, Shendye A, Rao M (1999) Molecular and biotechnological aspects of xylanases. FEMS Microbiol Rev 23:411–456 PubMed DOI

Lokhandwala J, Hopkins HC, Rodriguez-Iglesias A, Dattenbock C, Schmoll M, Zoltowski BD (2015) Structural biochemistry of a fungal LOV domain photoreceptor reveals an evolutionarily conserved pathway integrating light and oxidative stress. Structure 23:116–125 PubMed DOI

Maqsood A, Rehman A, Ahmad I, Nafees M, Ashraf I, Qureshi R, Jamil I, Rafay M, Hussain T (2014) Physiological attributes of fungi associated with stem end rot of mango (Mangifera indica L.) cultivars in postharvest fruit losses. Pak J Bot 46:1915–1920

Martinez-Soto D, Ruiz-Herrera J (2017) Functional analysis of the MAPK pathways in fungi. Rev Iberoam Micol 34:192–202 PubMed DOI

Miyake T, Mori A, Kii T, Okuno T, Usui Y, Sato F, Sammoto H, Watanabe A, Kariyama M (2005) Light effects on cell development and secondary metabolism in Monascus. J Ind Microbiol Biotechnol 32:103–108 PubMed DOI

Mooney JL, Yager LN (1990) Light is required for conidiation in Aspergillus nidulans. Genes Dev 4:1473–1482 PubMed DOI

Morosoli R, Durand S, Boucher F (1989) Stimulation of xylanase synthesis in Cryptococcus albidus by cyclic AMP. FEMS Microbiol Lett 57:57–60 DOI

Murthy PS, Suzuki S, Kusumoto KI (2015) Effect of light on the growth and acid protease production of Aspergillus oryzae. Food Sci Technol 21:631–635

Nielsen JC, Nielsen J (2017) Development of fungal cell factories for the production of secondary metabolites: linking genomics and metabolism. Synth Syst Biotechnol 2:5–12 PubMed DOI PMC

Nogueira KMV, Costa MDN, Paule RGD, Mendonca-Natividade FC, Ricci-Azevedo R, Silva RN (2015) Evidence of cAMP involvement in cellobiohydrolase expression and secretion by Trichoderma reesei in presence of the inducer sophorose. BMC Microbiol 15:195. https://doi.org/10.1186/s12866-015-0536-z PubMed DOI PMC

Paranagama PA, Wijeratne EMK, Burn AM, Marron MT, Gunatilaka MK, Arnold AE, Gunatilaka AAL (2007) Heptaketides from Corynespora sp. inhabiting cavern beard lichen, Usnea cavernosa: first report of metabolites of and endolichenic fungus. J Nat Prod 70:1700–1705 PubMed DOI

Pawlik A, Ruminowicz-Stefaniuk M, Frac M, Mazur A, Wielbo J, Janusz G (2019) The wood decay fungus Cerrena unicolor adjusts its metabolism to grow on various types of wood and light conditions. Plos One 14:e0211744. https://doi.org/10.1371/journal.pone.0211744

Purschwitz J, Muller S, Kastner C, Fischer R (2006) Seeing the rainbow: light sensing in fungi. Curr Opin Microbiol 9:566–571 PubMed DOI

Rozalska M, Mikucki J (1992) Staphylococcal L-asparaginase: catabolic repression of synthesis. Pol J Microbiol 41:145–150

Santiago KAA, Dela Cruz TEED, Ting ASY (2021) Diversity and bioactivity of endolichenic fungi in Usnea lichens of the Philippines. Czech Mycol 73:1–19 DOI

Schreckenbach T, Walckhoff B, Verfuerth C (1981) Blue light receptor in a white mutant of Physarum polycephalum mediates inhibition of spherulation and regulation of glucose metabolism. PNAS 78:1009–1013 PubMed DOI PMC

Schumacher J (2017) How light affects the life of Botrytis. Fungal Genet Biol 106:26–41 PubMed DOI

Sekiguchi J, Gaucher M (1977) Conidiogenesis and secondary metabolism in Penicillum urticae. Appl Environ Microbiol 33:147–158 PubMed DOI PMC

Soumya K, Swathi L, Sreelatha GL, Sharmila T (2014) Light influences pigment, biomass and morphology in Chaetomium cupreum- SS02- a photoresponse study. Int J Curr Microbiol Appl Sci 3:53–64

Sridevi B, Charya MAS (2011) Isolation, identification and screening of potential cellulase-free xylanase producing fungi. Afr J Biotechnol 10:4624–4630

Stappler E, Dattenbock C, Tisch D, Schmoll M (2017) Analysis of light and carbon specific transcriptomes implicates a class of G-protein-coupled receptors in cellulose sensing. mSphere 2:e00089–17. https://doi.org/10.1128/mSphere.00089-17

Sunitha VH, Ramesha A, Savitha J, Srinivas C (2012) Amylase production by endophytic fungi Cylindocephalum sp. isolated from medicinal plant Alpinia calcarate. Braz J Micriobiol 43:1213–1221 DOI

Takano Y, Kikuchi T, Kubo Y, Hamer JE, Mise K, Furusawa I (2000) The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol Plant Microbe Interact 13:374–383 PubMed DOI

Tan KK, Epton AH (1973) Effect of light on the growth and sporulation of Botrytis cinerea. Trans Br Mycol Soc 61:145–157 DOI

Tisch D, Schmoll M (2010) Light regulation of metabolic pathway in fungi. Appl Microbiol 85:1259–1277

Velmurugan P, Lee YH, Venil CK, Perumalsamy L, Chae JC, Oh BT (2010) Effect of light on growth, intracellular and extracellular pigment production by five pigment-producing filamentous fungi in synthetic medium. J Biosci Bioeng 109:346–350 PubMed DOI

Wang LL, Dai Y, Chen WP, Shao YC, Chen FS (2016a) Effects of light intensity and color on the biomass, extracellular red pigments, and citrinin production of Monascus ruber. J Agric Food Chem 64:9506–9514 PubMed DOI

Wang Z, Li N, Li JG, Dunlap JC, Trail F, Townsend JP (2016b) The fast-evolving phy-2 gene modulates sexual development in response to light in the model fungus Neurospora crassa. mBio 7:e02148. https://doi.org/10.1128/mBio.02148-15

Yap LS, Lee WL, Ting ASY (2021) Optimization of L-asparaginase production from endophytic Fusarium proliferatum using OFAT and RSM and its cytotoxic evaluation. J Microbiol Methods 191:e106358. https://doi.org/10.1016/j.mimet.2021.106358

Yu ZZ, Fischer R (2019) Light sensing and responses in fungi. Nat Rev 17:25–36

Zhang XX, Gao YY, Yin Y, Cai MH, Zhou XS, Zhang YX (2017) Regulation of different polyketide biosynthesis by green light in an endophytic fungus of mangrove leaf. 3 Biotech 7:363. https://doi.org/10.1007/s13205-017-0996-y

Zhu JC, Wang XJ (2005) Effect of blue light on conidiation development and glucoamylase enhancement in Aspergillus niger. Wei Sheng Wu Xue Bao 45:275–278 PubMed