DOI QR코드

DOI QR Code

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

Abstract

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.

극지에 서식하는 세균은 강한 빛과 자외선을 받는다. 이 연구에서 우리는 북극에 서식하는 지의류 Cetraria sp.에서 분리한 호냉성 세균 Sphingomonas sp. PAMC 26621의 생장에 빛이 미치는 영향을 조사하였다. 이 세균은 암조건에서 명조건에서 보다 생장이 느렸다. 놀랍게도, 이 세균은 M9 최소배지에 티아민 혹은 아스코브르산을 첨가하면 명조건에서 생장이 증가하였지만, N-acetylcysteine을 첨가한 배지에서는 생장의 변화가 없었다. 첨가한 티아민과 아스코브르산은 포도당-6 인산 탈수소효소와 항산화 효소의 활성을 증가시켰다. 이 연구의 결과는 지의류와의 공생에서 제공된 티아민이 Sphingomonas sp. PAMC26621의 빛에 의한 산화적 스트레스를 완화시키는 항산화제 역할을 함을 의미한다. 이 연구는 강한 빛과 자외선이 만연한 북극에 서식하는 세균에 대한 생리적, 생화학적 관점에서 고찰할 점을 제시한다.

Keywords

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.

References

  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. https://doi.org/10.1128/AEM.00597-06
  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. https://doi.org/10.1021/bi0118557
  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. https://doi.org/10.1111/j.1758-2229.2011.00272.x
  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. https://doi.org/10.1038/nrmicro2281
  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. https://doi.org/10.1093/oxfordjournals.pcp.a029186
  6. Charles KS and Peter RM. 2001. Molecular mechanisms of thiamine utilization. Curr. Mol. Med. 1, 197-207. https://doi.org/10.2174/1566524013363870
  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. https://doi.org/10.1002/embr.201338170
  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. https://doi.org/10.1657/1938-4246-42.4.396
  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. https://doi.org/10.1016/j.micpath.2017.02.030
  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. https://doi.org/10.4161/oxim.2.4.9112
  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. https://doi.org/10.1111/j.1365-3040.1994.tb00146.x
  12. Frei B. 1994. Reactive oxygen species and antioxidant vitamins: Mechanisms of action. Am. J. Med. 97, S5-S13. https://doi.org/10.1016/0002-9343(94)90292-5
  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. https://doi.org/10.1080/00984100050131323
  14. Goswami M and Jawali N. 2010. N-acetylcysteine-mediated modulation of bacterial antibiotic susceptibility. Antimicrob. Agents Chemother. 54, 3529-3530. https://doi.org/10.1128/AAC.00710-10
  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. https://doi.org/10.1038/ismej.2014.138
  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. https://doi.org/10.1016/j.phymed.2005.09.008
  17. Halliwell B. 1996. Vitamin C: antioxidant or pro-oxidant in vivo? Free Radic. Res. 25, 439-454. https://doi.org/10.3109/10715769609149066
  18. Hauruseu D and Koblizek M. 2012. Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl. Environ. Microbiol. 78, 7414-7419. https://doi.org/10.1128/AEM.01747-12
  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. https://doi.org/10.1111/j.1462-2920.2011.02560.x
  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. https://doi.org/10.1128/JB.00517-12
  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. https://doi.org/10.33073/pjm-2014-042
  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. https://doi.org/10.1074/jbc.274.20.13908
  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. https://doi.org/10.1099/mic.0.000461
  25. Kosanic M, Rankovic B, and Vukojevic J. 2011. Antioxidant properties of some lichen species. J. Food Sci. Technol. 48, 584-590. https://doi.org/10.1007/s13197-010-0174-2
  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. https://doi.org/10.1073/pnas.0407716102
  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. https://doi.org/10.1007/s11274-014-1695-z
  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. https://doi.org/10.1128/JB.00395-12
  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. https://doi.org/10.1002/lsm.20948
  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. https://doi.org/10.1371/journal.pone.0032156
  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. https://doi.org/10.1089/ast.2014.1278
  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. https://doi.org/10.1085/jgp.40.5.653
  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. https://doi.org/10.3164/jcbn.40.42
  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. https://doi.org/10.1073/pnas.1612360114
  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. https://doi.org/10.1074/jbc.274.5.2750
  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. https://doi.org/10.1016/S1357-2725(98)00095-8
  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. https://doi.org/10.1099/mic.0.000069
  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. https://doi.org/10.1098/rstb.2005.1764
  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. https://doi.org/10.1104/pp.109.140046
  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. https://doi.org/10.1128/AEM.71.11.6508-6514.2005
  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. https://doi.org/10.1096/fj.09-136572