DOI QR코드

DOI QR Code

Isolation and Identification of Alkali-tolerant Bacteria from Near-Shore Soils in Dokdo Island

  • Received : 2018.07.28
  • Accepted : 2018.09.20
  • Published : 2019.03.28

Abstract

Saline or alkaline condition in soil inhibits growth of most crop plants and limits crop yields in many parts of the world. Augmenting an alkaline soil with alkali-tolerant bacteria capable of promoting plant growth can be a promising approach in expanding fertile agricultural land. Near-shore environments of Dokdo Island, a remote island located in the middle of the East Sea, appear to have patches of seawater-influenced haloalkaline soil that is unsupportive for growth of conventional plants. To exploit metabolic capacities of alkali-tolerant bacteria for promoting plant growth in saline or alkaline soils, we isolated of alkali-tolerant bacteria from near-shore soil samples in Dokdo and investigated properties of the isolates. Alkali-tolerant bacteria were selectively cultivated by inoculating suspended and diluted soil samples on a plate medium adjusted to pH 10. Fifty colonies were identified based on their $GTG_5$-PCR genomic fingerprints and 16S rRNA gene sequences. Most isolates were affiliated to alkali-tolerant and/or halotolerant genera or species of the phyla Firmicutes (68%), Proteobacteria (30%) and Actinobacteria (2%). Unlike the typical soil bacterial flora in the island, alkali-tolerant isolates belonged to only certain taxa of terrestrial origin under the three phyla, which have traits of plant growth promoting activities including detoxification, phytohormone production, disease/pest control, nitrogen-fixation, phosphate solubilization or siderophore production. However, Firmicutes of marine origin generally dominated the alkali-tolerant community. Results of this study suggest that haloalkaline environments like Dokdo shore soils are important sources for plant growth promoting bacteria that can be employed in bio-augmentation of vegetation-poor alkaline soils.

Keywords

References

  1. Bolan N, Brennan R. 2011. Bioavailability of N, P, K, Ca, Mg, S, Si, and Micronutrients, pp. 11-80. In Huang PM, Li Y, Sumner ME (eds.), Handbook of Soil Sciences: Resource Management and Environmental Impacts, 2nd Ed. CRC Press, Boca Raton, FL.
  2. Thomas MD. 1955. Effect of ecological factors on photosynthesis. Annu. Rev. Plant Physiol. 6: 135-156. https://doi.org/10.1146/annurev.pp.06.060155.001031
  3. Li C, Fang B, Yang C, Shi D, Wang D. 2009. Effects of various saltalkaline mixed stresses on the state of mineral elements in nutrient solutions and growth of alkali resistant halophyte Chloris virgata. J. Plant Nutr. 32: 1137-1147. https://doi.org/10.1080/01904160902943163
  4. Gokbulak F, Ozcan M. 2008. Hydro-physical properties of soils developed from different parent materials. Geoderma 145: 376-380. https://doi.org/10.1016/j.geoderma.2008.04.006
  5. Marquez M, Sanchez-Porro C, Ventosa A. 2011. Halophilic and Haloalkaliphilic, Aerobic Endospore-forming Bacteria in Soil, pp. 309-339. In Logan NA, De Vos P (eds.), Endospore-Forming Soil Bacteria, 1st Ed. Springer-Verlag Berlin Heidelberg.
  6. Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ. 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 463-499. https://doi.org/10.1146/annurev.arplant.51.1.463
  7. Yang CW, Xu HH, Wang LL, Liu J, Shi DC, Wang DL. 2009. Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47: 79-86. https://doi.org/10.1007/s11099-009-0013-8
  8. Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 103: 626-631. https://doi.org/10.1073/pnas.0507535103
  9. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, et al. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1: 283-290. https://doi.org/10.1038/ismej.2007.53
  10. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, et al. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4: 1340-1351. https://doi.org/10.1038/ismej.2010.58
  11. J. Kemmitt S, Wright D, Goulding K, Jones D. 2006. pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biol. Biochem. 38: 898-911. https://doi.org/10.1016/j.soilbio.2005.08.006
  12. Van der Heijden MG, Bardgett RD, Van Straalen NM. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11: 296-310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
  13. Eisenhauer N, Bessler H, Engels C, Gleixner G, Habekost M, Milcu A, et al. 2010. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91: 485-496. https://doi.org/10.1890/08-2338.1
  14. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, et al. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 4927-4932. https://doi.org/10.1073/pnas.0730845100
  15. Sohn YK. 1995. Geology of Tok Island, Korea: eruptive and depositional processes of a shoaling to emergent island volcano. Bull. Volcanol. 56: 660-674. https://doi.org/10.1007/BF00301469
  16. Joshi P, Bhatt A. 2011. Diversity and function of plant growth promoting rhizobacteria associated with wheat rhizosphere in North Himalayan region. Int. J. Environ. Sci. 1: 1135.
  17. Farina R, Beneduzi A, Ambrosini A, de Campos SB, Lisboa BB, Wendisch V, et al. 2012. Diversity of plant growth-promoting rhizobacteria communities associated with the stages of canola growth. Appl. Soil Ecol. 55: 44-52. https://doi.org/10.1016/j.apsoil.2011.12.011
  18. Chang KI, Kim YB, Suk MS, Byun SK. 2002. Hydrography around Dokdo. Ocean Polar Res. 24: 369-389. https://doi.org/10.4217/OPR.2002.24.4.369
  19. Lee GS, Choo YS. 2009. Physical and chemical characteristics of Dokdo Soil. J. Ecol. Environ. 32: 295-304. https://doi.org/10.5141/JEFB.2009.32.4.295
  20. Enache M, Popescu G, Itoh T, Kamekura M. 2012. Halophilic Microorganisms from Man-made and Natural Hypersaline Environments: Physiology, Ecology, and Biotechnological Potential, pp. 201-226. In Stan-Lotter H, Fendrihan S (eds.), Adaption of Microbial Life to Environmental Extremes: Novel Research Results and Application, 2nd Ed. Springer, Cham, Vienna.
  21. Collins MD, Lund BM, Farrow JAE, Schleifer KH. 1983. Chemotaxonomic study of an alkalophilic bacterium, Exiguobacterium aurantiacum gen. nov., sp. nov. J. Gen. Microbiol. 129: 2037-2042.
  22. Ishikawa M, Nakajima K, Yanagi M, Yamamoto Y, Yamasato K, Toffin L, et al. 2003. Marinilactibacillus psychrotolerans gen. nov., sp. nov., a halophilic and alkaliphilic marine lactic acid bacterium isolated from marine organisms in temperate and subtropical areas of Japan. Int. J. Syst. Evol. Microbiol. 53: 711-720. https://doi.org/10.1099/ijs.0.02446-0
  23. Crapart S, Fardeau ML, Cayol JL, Thomas P, Sery C, Ollivier B, et al. 2007. Exiguobacterium profundum sp. nov., a moderately thermophilic, lactic acid-producing bacterium isolated from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 57: 287-292. https://doi.org/10.1099/ijs.0.64639-0
  24. Yokoi H, Aratake T, Hirose J, Hayashi S, Takasaki Y. 2001. Simultaneous production of hydrogen and bioflocculant by Enterobacter sp. BY-29. World J. Microbiol. Biotechnol. 17: 609-613. https://doi.org/10.1023/A:1012463508364
  25. Muslim SN, Mohammed Ali AN, Al-Kadmy IMS, Khazaal SS, Ibrahim SA, Al-Saryi NA, et al. 2018. Screening, nutritional optimization and purification for phytase produced by Enterobacter aerogenes and its role in enhancement of hydrocarbons degradation and biofilm inhibition. Microb. Pathog. 115: 159-167. https://doi.org/10.1016/j.micpath.2017.12.047
  26. Wada M, Yoshizumi A, Furukawa Y, Kawabata H, Ueda M, Takagi H, et al. 2004. Cloning and overexpression of the Exiguobacterium sp. F42 gene encoding a new short chain dehydrogenase, which catalyzes the stereoselective reduction of ethyl 3-oxo-3-(2-thienyl) propanoate to ethyl (S)-3-hydroxy-3-(2-thienyl)propanoate. Biosci. Biotechnol. Biochem. 68: 1481-1488. https://doi.org/10.1271/bbb.68.1481
  27. Hwang BY, Kim JH, Kim J, Kim BG. 2005. Screening of Exiguobacterium acetylicum from soil samples showing enantioselective and alkalotolerant esterase activity. Biotechnol. Bioprocess Eng. 10: 367. https://doi.org/10.1007/BF02931857
  28. Kasana RC, Yadav SK. 2007. Isolation of a psychrotrophic Exiguobacterium sp. SKPB5 (MTCC 7803) and characterization of its alkaline protease. Curr. Microbiol. 54: 224-229. https://doi.org/10.1007/s00284-006-0402-1
  29. Toffin L, Zink K, Kato C, Pignet P, Bidault A, Bienvenu N, et al. 2005. Marinilactibacillus piezotolerans sp. nov., a novel marine lactic acid bacterium isolated from deep sub-seafloor sediment of the Nankai Trough. Int. J. Syst. Evol. Microbiol. 55: 345-351. https://doi.org/10.1099/ijs.0.63236-0
  30. Son JS, Sumayo M, Hwang YJ, Kim BS, Ghim SY. 2014. Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl. Soil Ecol. 73: 1-8. https://doi.org/10.1016/j.apsoil.2013.07.016
  31. Kim YE, Yoon H, Kim M, Nam YJ, Kim H, Seo Y, et al. 2014. Metagenomic analysis of bacterial communities on Dokdo Island. J. Gen. Appl. Microbiol. 60: 65-74. https://doi.org/10.2323/jgam.60.65
  32. You YH, Park JM, Lee MC, Kim JG. 2015. Characterization and phylogenetic analysis of halophilic bacteria isolated from rhizosphere soils of coastal plants in Dokdo Islands. Korean J. Microbiol. 51: 86-95. https://doi.org/10.7845/kjm.2015.5008
  33. Vaz-Moreira I, Egas C, Nunes OC, Manaia CM. 2011. Culturedependent and culture-independent diversity surveys target different bacteria: a case study in a freshwater sample. Antonie van Leeuwenhoek. 100: 245-257. https://doi.org/10.1007/s10482-011-9583-0
  34. Mwirichia R, Muigai AW, Tindall B, Boga HI, Stackebrandt E, Mwirichia R, et al. 2010. Isolation and characterisation of bacteria from the haloalkaline Lake Elmenteita, Kenya. Extremophiles 14: 339-348. https://doi.org/10.1007/s00792-010-0311-x
  35. Mwirichia R, Cousin S, Muigai AW, Boga HI, Stackebrandt E. 2011. Bacterial diversity in the haloalkaline Lake Elmenteita, Kenya. Curr. Microbiol. 62: 209-221. https://doi.org/10.1007/s00284-010-9692-4
  36. Keshri J, Mishra A, Jha B. 2013. Microbial population index and community structure in saline-alkaline soil using gene targeted metagenomics. Microbiol Res. 168: 165-173. https://doi.org/10.1016/j.micres.2012.09.005
  37. Ma B, Gong J. 2013. A meta-analysis of the publicly available bacterial and archaeal sequence diversity in saline soils. World J. Microbiol. Biotechnol. 29: 2325-2334. https://doi.org/10.1007/s11274-013-1399-9
  38. Panosyan H, Hakobyan A, Birkeland NK, Trchounian A. 2018. Bacilli community of saline-alkaline soils from the Ararat Plain (Armenia) assessed by molecular and culture-based methods. Syst. Appl. Microbiol. 41: 232-240. https://doi.org/10.1016/j.syapm.2017.12.002
  39. Ahmad F, Ahmad I, Khan MS. 2008. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol. Res. 163: 173-181. https://doi.org/10.1016/j.micres.2006.04.001
  40. Phi QT, Park YM, Seul KJ, Ryu CM, Park SH, Kim JG, et al. 2010. Assessment of root-associated paenibacillus polymyxa groups on growth promotion and induced systemic resistance in pepper. J. Microbiol. Biotechnol. 20: 1605-1613. https://doi.org/10.4014/jmb.1007.07014
  41. Pramanik K, Mitra S, Sarkar A, Maiti TK. 2018. Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain Enterobacter aerogenes MCC 3092. J. Hazard. Mater. 351: 317-329. https://doi.org/10.1016/j.jhazmat.2018.03.009
  42. Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S, et al. 2018. A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res. Microbiol. 169: 20-32. https://doi.org/10.1016/j.resmic.2017.08.005
  43. Zhang S, Reddy M, Kloepper JW. 2002. Development of assays for assessing induced systemic resistance by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol. Control. 23: 79-86. https://doi.org/10.1006/bcon.2001.0992
  44. Valencia-Cantero E, Hernandez-Calderon E, Velazquez-Becerra C, Lopez-Meza JE, Alfaro-Cuevas R, Lopez-Bucio J. 2007. Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common bean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant Soil. 291: 263-273. https://doi.org/10.1007/s11104-007-9191-y
  45. Compant S, Duffy B, Nowak J, Clement C, Barka EA. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71: 4951-4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005
  46. Egidi E, Wood JL, Mathews E, Fox E, Liu W, Franks AE. 2016. Draft genome sequence of Bacillus cereus LCR12, a plant growth-promoting rhizobacterium isolated from a heavy metal-contaminated environment. Genome Announc. 4: e01041-16.
  47. Yang LL, Huang Y, Liu J, Ma L, Mo MH, Li WJ, et al. 2012. Lysinibacillus mangiferahumi sp. nov., a new bacterium producing nematicidal volatiles. Antonie van Leeuwenhoek. 102: 53-59. https://doi.org/10.1007/s10482-012-9712-4
  48. Luo X, Zhang J, Li D, Xin Y, Xin D, Fan L. 2014. Planomicrobium soli sp. nov., isolated from soil. Int. J. Syst. Evol. Microbiol. 64: 2700-2705. https://doi.org/10.1099/ijs.0.055426-0
  49. Upadhyay SK, Singh JS, Singh DP. 2011. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 21: 214-222. https://doi.org/10.1016/S1002-0160(11)60120-3
  50. Kumar KV, Srivastava S, Singh N, Behl HM. 2009. Role of metal resistant plant growth promoting bacteria in ameliorating fly ash to the growth of Brassica juncea. J. Hazard. Mater. 170: 51-57. https://doi.org/10.1016/j.jhazmat.2009.04.132
  51. Waranusantigul P, Lee H, Kruatrachue M, Pokethitiyook P, Auesukaree C. 2011. Isolation and characterization of lead-tolerant Ochrobactrum intermedium and its role in enhancing lead accumulation by Eucalyptus camaldulensis. Chemosphere 85: 584-590. https://doi.org/10.1016/j.chemosphere.2011.06.086