Novel insight into the role of thiamine for the growth of a lichen-associated Arctic bacterium, Sphingomonas sp., in the light

Sphingomonas 속 세균의 명조건 생장에서 티아민의 필수적인 역할

  • Pham, Nhung (Department of Biomedical Science and Center for Bio-Nanomaterials, Daegu University) ;
  • Pham, Khoi (Department of Biomedical Science and Center for Bio-Nanomaterials, Daegu University) ;
  • Lee, ChangWoo (Department of Biomedical Science and Center for Bio-Nanomaterials, Daegu University) ;
  • Jang, Sei-Heon (Department of Biomedical Science and Center for Bio-Nanomaterials, Daegu University)
  • 팜눙 (대구대학교 의생명과학과) ;
  • 팜코이 (대구대학교 의생명과학과) ;
  • 이창우 (대구대학교 의생명과학과) ;
  • 장세헌 (대구대학교 의생명과학과)
  • Received : 2019.01.28
  • Accepted : 2019.03.14
  • Published : 2019.03.31


Bacteria in the polar region are under strong light and ultraviolet radiation. In this study, we investigated the effects of light on the growth of a psychrophilic bacterium, Sphingomonas sp. PAMC 26621, isolated from an Arctic lichen Cetraria sp. The growth of the strain in the light was lower than that in the dark. Surprisingly, thiamine increased the growth of Sphingomonas sp. PAMC 26621 in M9 minimal medium under light conditions. Thiamine increased the growth of the strain in a concentration-dependent manner along with ascorbic acid. N-acetylcysteine had no effect on the growth of the strain in the light. Thiamine and ascorbic acid also increased the activities of glucose-6-phosphate dehydrogenase and superoxide dismutase. The results of this study indicate that thiamine provided by the lichen symbiosis system plays an important role in light-induced oxidative stress in this Arctic bacterium as an antioxidant. Our study provide insight into the biochemistry and physiology of Arctic bacteria under strong light and ultraviolet radiation.


Sphingomonas sp. PAMC 26621;ascorbic acid;light;NADPH;thiamine

MSMHBQ_2019_v55n1_17_f0001.png 이미지

Fig. 1. The growth of Sphingomonas sp. PAMC 26621 in M9 medium and MT medium under light condition (A) and dark condition (B).

MSMHBQ_2019_v55n1_17_f0002.png 이미지

Fig. 2. The effects of antioxidants on the growth of Sphingomonas sp. PAMC 26621.

MSMHBQ_2019_v55n1_17_f0003.png 이미지

Fig. 3. Activities of G6PDH at mid-log and stationary phase on MT medium, M9 + thiamine, M9 + ascorbic acid, M9 (light), M9 (dark) (A).

MSMHBQ_2019_v55n1_17_f0004.png 이미지

Fig. 4. Native polyacrylamide gel stained for SOD activity of samples from Sphingomonas sp. PAMC 26621.


Supported by : Daegu University


  1. Alonso-Saez L, Gasol JM, Lefort T, Hofer J, and Sommaruga R. 2006. Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl. Environ. Microbiol. 72, 5806-5813.
  2. Arjunan P, Nemeria N, Brunskill A, Chandrasekhar K, Sax M, Yan Y, Jordan F, Guest JR, and Furey W. 2002. Structure of the pyruvate dehydrogenase multienzyme complex E1 component from Escherichia coli at 1.85 A resolution. Biochemistry 41, 5213-5221.
  3. Cardinale M, Steinova J, Rabensteiner J, Berg G, and Grube M. 2012. Age, sun and substrate: triggers of bacterial communities in lichens. Environ. Microbiol. Rep. 4, 23-28.
  4. Cary SC, McDonald IR, Barrett JE, and Cowan DA. 2010. On the rocks: the microbiology of Antarctic dry valley soils. Nat. Rev. Microbiol. 8, 129-138.
  5. Casano LM, Gomez LD, Lascano HR, Gonzalez CA, and Trippi VS. 1997. Inactivation and degradation of CuZn-SOD by active oxygen ppecies in wheat chloroplasts exposed to photooxidative stress. Plant Cell Physiol. 38, 433-440.
  6. Charles KS and Peter RM. 2001. Molecular mechanisms of thiamine utilization. Curr. Mol. Med. 1, 197-207.
  7. De Maayer P, Anderson D, Cary C, and Cowan DA. 2014. Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep. 15, 508-517.
  8. Dieser M, Greenwood M, and Foreman CM. 2010. Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct. Antarct. Alp. Res. 42, 396-405.
  9. Eroshenko D, Polyudova T, and Korobov V. 2017. N-acetylcysteine inhibits growth, adhesion and biofilm formation of Gram-positive skin pathogens. Microb. Pathog. 105, 145-152.
  10. Flora SJS. 2009. Structural, chemical and biological aspects of antioxidants for strategies against metal and metalloid exposure. Oxid. Med. Cell. Longev. 2, 191-206.
  11. Foyer CH, DescourviERes P, and Kunert KJ. 1994. Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ. 17, 507-523.
  12. Frei B. 1994. Reactive oxygen species and antioxidant vitamins: Mechanisms of action. Am. J. Med. 97, S5-S13.
  13. Fu YC, Jin XP, Wei SM, Lin HF, and Kacew S. 2000. Ultraviolet radiation and reactive oxygen generation as inducers of keratinocyte apoptosis: protective role of tea polyphenols. J. Toxicol. Environ. Health A 61, 177-188.
  14. Goswami M and Jawali N. 2010. N-acetylcysteine-mediated modulation of bacterial antibiotic susceptibility. Antimicrob. Agents Chemother. 54, 3529-3530.
  15. Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, et al. 2015. Exploring functional contexts of symbiotic sustain within lichenassociated bacteria by comparative omics. ISME J. 9, 412-424.
  16. Gulluce M, Aslan A, Sokmen M, Sahin F, Adiguzel A, Agar G, and Sokmen A. 2006. Screening the antioxidant and antimicrobial properties of the lichens Parmelia saxatilis, Platismatia glauca, Ramalina pollinaria, Ramalina polymorpha, and Umbilicaria nylanderiana. Phytomedicine 13, 515-521.
  17. Halliwell B. 1996. Vitamin C: antioxidant or pro-oxidant in vivo? Free Radic. Res. 25, 439-454.
  18. Hauruseu D and Koblizek M. 2012. Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl. Environ. Microbiol. 78, 7414-7419.
  19. Hodkinson BP, Gottel NR, Schadt CW, and Lutzoni F. 2012. Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ. Microbiol. 14, 147-161.
  20. Jang SH, Kim J, Kim J, Hong S, and Lee C. 2012. Genome sequence of cold-adapted Pseudomonas mandelii strain JR-1. J. Bacteriol. 194, 3263.
  21. Kim MK, Park H, and Oh TJ. 2013. Antioxidant properties of various microorganisms isolated from Arctic lichen Stereocaulon spp. Korean J. Microbiol. Biotechnol. 8, 350-357.
  22. Kim MK, Park H, and Oh TJ. 2014. Antibacterial and antioxidant capacity of polar microorganisms isolated from Arctic lichen Ochrolechia sp. Pol. J. Microbiol. 63, 317-322.
  23. Kirkman HN, Rolfo M, Ferraris AM, and Gaetani GF. 1999. Mechanisms of protection of catalase by NADPH. Kinetics and stoichiometry. J. Biol. Chem. 274, 13908-13914.
  24. Kono M, Tanabe H, Ohmura Y, Satta Y, and Terai Y. 2017. Physical contact and carbon transfer between a lichen-forming Trebouxia alga and a novel Alphaproteobacterium. Microbiology 163, 678-691.
  25. Kosanic M, Rankovic B, and Vukojevic J. 2011. Antioxidant properties of some lichen species. J. Food Sci. Technol. 48, 584-590.
  26. Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, and Pfeifhofer HW. 2005. Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc. Natl. Acad. Sci. USA 102, 3141-3146.
  27. Lee YM, Kim EH, Lee HK, and Hong SG. 2014. Biodiversity and physiological characteristics of Antarctic and Arctic lichens-associated bacteria. World J. Microbiol. Biotechnol. 30, 2711-2721.
  28. Lee H, Shin SC, Lee J, Kim SJ, Kim BK, Hong SG, Kim EH, and Park H. 2012. Genome sequence of Sphingomonas sp. strain PAMC 26621, an Arctic-lichen-associated bacterium isolated from a Cetraria sp. J. Bacteriol. 194, 3030.
  29. Lipovsky A, Nitzan Y, Gedanken A, and Lubart R. 2010. Visible light-induced killing of bacteria as a function of wavelength: implication for wound healing. Lasers Surg. Med. 42, 467-472.
  30. Ma Q, Zhang W, Zhang L, Qiao B, Pan C, Yi H, Wang L, and Yuan YJ. 2012. Proteomic analysis of Ketogulonicigenium vulgare under glutathione reveals high demand for thiamin transport and antioxidant protection. PLoS One 7, e32156.
  31. Musilova M, Wright G, Ward JM, and Dartnell LR. 2015. Isolation of radiation-resistant bacteria from Mars analog Antarctic dry valleys by preselection, and the correlation between radiation and desiccation resistance. Astrobiology 15, 1076-1090.
  32. Ninfali P, Ditroilo M, Capellacci S, and Biagiotti E. 2001. Rabbit brain glucose-6-phosphate dehydrogenase: biochemical properties and inactivation by free radicals and 4-hydroxy-2-nonenal. Neuro-Report 12, 4149-4153.
  33. Northrop JH. 1957. The effect of ultraviolet and white light on growth rate, lysis, and phage production of Bacillus megatherium. J. Gen. Physiol. 40, 653-661.
  34. Okai Y, Higashi-Okai K, Sato EF, Konaka R, and Inoue M. 2007. Potent radical-scavenging activities of thiamin and thiamin diphosphate. J. Clin. Biochem. Nutr. 40, 42-48.
  35. Romine MF, Rodionov DA, Maezato Y, Anderson LN, Nandhikonda P, Rodionova IA, Carre A, Li X, Xu C, Clauss TR, et al. 2017. Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism. Proc. Natl. Acad. Sci. USA 114, E1205-E1214.
  36. Salvemini F, Franze A, Iervolino A, Filosa S, Salzano S, and Ursini MV. 1999. Enhanced glutathione levels and oxidoresistance mediated by increased glucose-6-phosphate dehydrogenase expression. J. Biol. Chem. 274, 2750-2757.
  37. Schenk G, Duggleby RG, and Nixon PF. 1998. Properties and functions of the thiamin diphosphate dependent enzyme transketolase. Int. J. Biochem. Cell Biol. 30, 1297-1318.
  38. Sigurbjornsdottir MA, Andresson OS, and Vilhelmsson O. 2015. Analysis of the Peltigera membranacea metagenome indicates that lichen-associated bacteria are involved in phosphate solubilization. Microbiology 161, 989-996.
  39. Stincone A, Prigione A, Cramer T, Wamelink MM, Campbell K, Cheung E, Olin-Sandoval V, Gruning N, Kruger A, Tauqeer Alam M, et al. 2014. The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol. Rev. Camb. Philos. Soc. 90, 927-963.
  40. Tretter L and Adam-Vizi V. 2005. Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 2335-2345.
  41. Tunc-Ozdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, and Shintani D. 2009. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol. 151, 421-432.
  42. Weissman L, Garty J, and Hochman A. 2005. Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydration. Appl. Environ. Microbiol. 71, 6508-6514.
  43. Zhang Z, Liew CW, Handy DE, Zhang Y, Leopold JA, Hu J, Guo L, Kulkarni RN, Loscalzo J, and Stanton RC. 2010. High glucose inhibits glucose-6-phosphate dehydrogenase, leading to increased oxidative stress and beta-cell apoptosis. FASEB J. 24, 1497-1505.