Advertisement

3 Biotech

, 9:46 | Cite as

Biostimulation potentials of corn steep liquor in enhanced hydrocarbon degradation in chronically polluted soil

  • Lateef B. SalamEmail author
  • Aisha Ishaq
Original Article
  • 12 Downloads

Abstract

The effects of corn steep liquor (CSL) on hydrocarbon degradation and microbial community structure and function was evaluated in field-moist soil microcosms. Chronically polluted soil treated with CSL (AB4) and an untreated control (3S) was compared over a period of 6 weeks. Gas chromatographic fingerprints of residual hydrocarbons revealed removal of 95.95% and 94.60% aliphatic and aromatic hydrocarbon fractions in AB4 system with complete disappearance of nC1–nC8, nC10, nC15, nC20–nC23 aliphatics and aromatics such as naphthalene, acenaphthylene, fluorene, phenanthrene, pyrene, benzo(a)anthracene, and indeno(123-cd)pyrene in 42 days. In 3S system, there is removal of 61.27% and 66.58% aliphatic and aromatic fractions with complete disappearance of nC2 and nC21 aliphatics and naphthalene, acenaphthylene, fluorene, phenanthrene, pyrene, and benzo(a)anthracene aromatics in 42 days. Illumina shotgun sequencing of the DNA extracted from the two systems showed the preponderance of Actinobacteria (31.46%) and Proteobacteria (38.95%) phyla in 3S and AB4 with the dominance of Verticillium (22.88%) and Microbacterium (8.16%) in 3S, and Laceyella (24.23%), Methylosinus (8.93%) and Pedobacter (7.73%) in AB4. Functional characterization of the metagenomic reads revealed diverse metabolic potentials and adaptive traits of the microbial communities in the two systems to various environmental stressors. It also revealed the exclusive detection of catabolic enzymes in AB4 system belonging to the aldehyde dehydrogenase superfamily. The results obtained in this study showed that CSL is a potential resource for bioremediation of hydrocarbon-polluted soils.

Keywords

Corn steep liquor Hydrocarbon-polluted soil Soil microcosm Illumina shotgun sequencing Microbial community structure Bioremediation 

Supplementary material

13205_2019_1580_MOESM1_ESM.docx (2.7 mb)
Supplementary material 1 (DOCX 2730 KB)

References

  1. Adebusoye SA, Ilori MO, Obayori OS, Oyetibo GO, Akindele KA, Amund OO (2010) Efficiency of cassava steep liquor for bioremediation of diesel oil-contaminated tropical agricultural soil. Environmentalist 30:23–24Google Scholar
  2. Alexander M (1999) Biodegradation and bioremediation, 2nd edn. Academic Press, San DiegoGoogle Scholar
  3. Amadi A, Bari YU (1992) Use of poultry manure for amendment of oil polluted soils in relation to the growth of maize (Zea mays). Environ Int 18:521–552Google Scholar
  4. Andrew RWJ, Jackson JM (1996) Pollution and waste management. In: The natural environment and human impact. Longman Publishers, Singapore, pp 281–297Google Scholar
  5. Aranda E (2016) Promising approaches towards biotransformation of polycyclic aromatic hydrocarbons with Ascomycota fungi. Curr Opin Biotechnol 38:1–8PubMedGoogle Scholar
  6. Atlas RM (1981) Microbial degradation of petroleum: an environmental perspective. Microbiol Rev 45:180–209PubMedPubMedCentralGoogle Scholar
  7. Bashir Y, Singh SP, Konwar BK (2014) Metagenomics: an application-based perspective. Chinese J Biol  https://doi.org/10.1155/2014/146030 CrossRefGoogle Scholar
  8. Bossert I, Bartha R (1984) The fate of fuel spills in soil ecosystems. In: Atlas RM (ed) Petroleum microbiology. Macmillan, New York, pp 435–473 InGoogle Scholar
  9. Bundy JG, Paton GI, Campbell CD (2002) Microbial communities in different soils do not converge after diesel contamination. J Appl Microbiol 92:276–288PubMedGoogle Scholar
  10. Carrillo L, Ahrendts MRB, Maldonado MJ (2009) Alkalithermophilic actinomycetes in a subtropical area of Jujuy, Argentina. Revista Argentina de Microbiología 41:112–116PubMedGoogle Scholar
  11. Chen J-J, Lin L-B, Zhang L-L, Zhang J, Tang S-K, Wei Y-L, Li W-J (2012) Laceyella sediminis sp. nov., a thermophilic bacterium isolated from a hot spring. Int J Syst Evol Microbiol 62:38–42PubMedGoogle Scholar
  12. Chiani M, Akbarzadeh A, Farhangi A, Mehrabi MR (2010) Production of desferrioxamine B (Desfaral) using corn steep liquor in Streptomyces pilosus. Pak J Biol Sci 13:1151–1155PubMedGoogle Scholar
  13. Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at a glance quality assessment of illumine second-generation sequencing data. BMC Bioinform 11:485Google Scholar
  14. DeFlaun MF, Ensley BD, Steffan RJ (1992) Biological oxidation of hydrochlorofluorocarbons (HCFCs) by a methanotrophic bacterium. Biotechnol 10:1576–1578Google Scholar
  15. Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903Google Scholar
  16. El-Sayed AK, Abou-Dobara MI, El-Fallal A, Omar NF (2017) Gene sequence, modeling, and enzymatic characterization of α-amylase AmyLa from the thermophile Laceyella sp. DS3. Starch 69(5–6):1–9Google Scholar
  17. Endo G, Narita M, Huang CC, Silver S (2002) Microbial heavy metal resistance transposons and plasmids: potential use for environmental biotechnology. J Environ Biotechnol 2:71–82Google Scholar
  18. Ensign JC (1992) Introduction to the actinomycetes. In: Ballows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) the Prokaryotes. a handbook on the biology of bacteria, ecophysiology, isolation, identification, application. Springer, New York, pp 811–815Google Scholar
  19. Esser D, Kouril T, Talfournier F et al (2013) Unravelling the function of paralogs of the aldehyde dehydrogenase super family from Sulfolobus solfataricus. Extremophiles 12:75–88Google Scholar
  20. Fedorak PM, Westlake DWS (1986) Fungal metabolism of n-alkylbenzenes. Appl Environ Microbiol 51(2):435–437PubMedPubMedCentralGoogle Scholar
  21. Fierer N, Bradford MA, Jackson RB (2007) Towards an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedGoogle Scholar
  22. Filipovic SS, Ristc MD, Sakac MB (2002) Technology of corn steep liquor application in animal mashes and their quality. Roum Biotechnol Lett 7:705–710Google Scholar
  23. Fox JL (2011) Natural-born eaters. Nat Biotechnol 29:103–106PubMedGoogle Scholar
  24. Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243PubMedGoogle Scholar
  25. Godoy P, Reina R, Calderón A, Wittich R-M, García-Romera I, Aranda E (2016) Exploring the potential of fungi isolated from PAH-polluted soil as a source of xenobiotics-degrading fungi. Environ Sci Polut Res.  https://doi.org/10.1007/s11356-016-7257-1 CrossRefGoogle Scholar
  26. Goldfarb KC, Karaoz U, Hanson CA et al (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:94PubMedPubMedCentralGoogle Scholar
  27. Graziano M, Rizzo C, Michaud L, Porporato EMD, De Domenico E, Spano N, Lo Giudice A (2016) Biosurfactant production by hydrocarbon degrading Brevibacterium and Vibrio isolates from the sea pen Pteroeides spinosum (Ellis, 1764). J Basic Microbiol 56(9):963–974PubMedGoogle Scholar
  28. Habe H, Chung JS, Lee JH, Kasuga K, Yoshida T, Nojiri H, Omori T (2001) Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by two types of bacteria having angular dioxygenases with different features. Appl Environ Microbiol 67:3610–3617PubMedPubMedCentralGoogle Scholar
  29. Habe H, Ashikawa Y, Saiki Y, Yoshida T, Nojiri H, Omori T (2002) Sphingomonas sp. strain KA1, carrying a carbazole dioxygenase gene homologue, degrades chlorinated dibenzo-p-dioxins in soil. FEMS Microbiol Lett 211:43–49PubMedGoogle Scholar
  30. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–678PubMedPubMedCentralGoogle Scholar
  31. Hanphakphoom S, Maneewong N, Sukkhum S, Tokuyama S, Kitpreechavanich V (2014) Characterization of poly(L-lactide)-degrading enzyme produced by thermophilic filamentous bacteria Laceyella sacchari LP175. J Gen Appl Microbiol 60:13–22PubMedGoogle Scholar
  32. Kachienga L, Jitendra K, Momba M (2018) Metagenomic profiling for assessing microbial diversity and microbial adaptation to degradation of hydrocarbons in two South African petroleum contaminated water aquifers. Sci Rep 8:7564PubMedPubMedCentralGoogle Scholar
  33. Kanaly RA, Harayama S (2010) Advances in the field of high molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microbiol Biotechnol 3(2):132–164Google Scholar
  34. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428(4):726–731PubMedGoogle Scholar
  35. Keegan KP, Glass EM, Meyer F (2016) MG-RAST, a metagenomics service for analysis of microbial community structure and function. Methods Mol Biol 1399:207–233PubMedGoogle Scholar
  36. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie-2. Nat Methods 9(4):357–359PubMedPubMedCentralGoogle Scholar
  37. Larkin MJ, Kulakov LA, Allen CC (2005) Biodegradation and Rhodococcus-masters of catabolic versatility. Curr Opin Biotechnol 16:282–290PubMedGoogle Scholar
  38. Lawford HG, Rousseau JD (1997) Corn steep liquor as a cost-effective nutrition adjunct in high performance Zymomonas ethanol fermentation. Appl Biochem Biotechnol 63–65:287–304PubMedGoogle Scholar
  39. Liggert RW, Koffler H (1948) Corn steep liquor in microbiology. Bacteriol Rev 12(4):297–311Google Scholar
  40. Lin C, Olson BH (1995) Occurrence of cop-like resistance genes among bacteria isolated from a water distribution system. Can J Microbiol 41:642–646Google Scholar
  41. Lomthong T, Chotineeranat S, Kitpreechavanich V (2015) Production and characterization of raw starch degrading enzyme from a newly isolated thermophilic filamentous bacterium, Laceyella sacchari LP175. Starch 67(3–4):255–266Google Scholar
  42. Maddipati P, Atiyeh HK, Bellmer DN, Huhnke RL (2011) Ethanol production from Syngas by Clostridium strain P11 using corn steep liquor as a nutrient replacement to yeast extract. Biores Technol 102:6494–6501Google Scholar
  43. Maier RM (2009) Microorganisms and organic pollutants. In: Maier RM, Pepper IL, Gerba CP (eds) Environmental microbiology, second edn. Academic Press, London, pp 387–420Google Scholar
  44. Maier RM, Pepper IL, Gerba CP (2000) Environmental microbiology. Academic Press, LondonGoogle Scholar
  45. Manickam N, Mau M, Schlo¨mann M (2006) Characterization of the novel HCH-degrading Microbacterium sp. ITRC1. Appl Microbiol Biotechnol 69:580–588PubMedGoogle Scholar
  46. Marchler-Bauer A, Derbyshire MK, Gonzales NR et al (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(D):222–226Google Scholar
  47. Margesin R, Zhang D-C (2013) Pedobacter ruber sp. nov., a psychrophilic bacterium isolated from soil. Int J Syst Evol Microbiol 63:339–344PubMedGoogle Scholar
  48. Morikawa M, Daido H, Takao T, Murata S, Shimonishi Y, Imanaka T (1993) A new lipopeptide biosurfactant produced by Arthrobacter sp. strain MIS38. J Bacteriol 175:6459–6466PubMedPubMedCentralGoogle Scholar
  49. Muangchinda C, Chavanich S, Viyakarn V, Watanabe K, Imura S, Vangnai AS, Pinyakong O (2015) Abundance and diversity of functional genes involved in the degradation of aromatic hydrocarbons in Antarctic soils and sediments around Syowa Station. Environ Sci Pollut Res 22:4725–4735Google Scholar
  50. Mutnuri S, Vasudevan N, Kaestner M (2005) Degradation of anthracene and pyrene supplied by microcrystals and nonaqueous-phase liquids. Appl Microbiol Biotechnol 67:569–576PubMedGoogle Scholar
  51. Nemergut DR, Martin AP, Schmidt SK (2004) Intergon diversity in heavy-metal-contaminated mine tailings and inferences about integron evolution. Appl Environ Microbiol 70:1160–1168PubMedPubMedCentralGoogle Scholar
  52. Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60:151–166PubMedPubMedCentralGoogle Scholar
  53. Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199PubMedGoogle Scholar
  54. Nojiri H, Nam J-W, Kosaka M et al (1999) Diverse oxygenations catalyzed by carbazole 1,9a-dioxygenase from Pseudomonas sp. strain CA10. J Bacterio 181(10):3105–3113Google Scholar
  55. Nojiri H, Habe H, Omori T (2001) Bacterial degradation of aromatic compounds via angular dioxygenations. J Gen Appl Microbiol 47:279–305PubMedGoogle Scholar
  56. Nucifora G, Chu L, Misra TK, Silver S (1989) Cadmium resistance from Staphylococcus aureus plasmid p1258 cadA gene results from cadmium-efflux ATPase. Proc Natl Acad Sci USA 86:3544–3548PubMedGoogle Scholar
  57. Obayori OS, Ilori MO, Adebusoye SA, Amund OO, Oyetibo GO (2008) Microbial population changes in tropical agricultural soil experimentally contaminated with crude petroleum. Afr J Biotechnol 7:4512–4520Google Scholar
  58. Obayori OS, Ilori MO, Adebusoye SA, Oyetibo GO, Omotayo AE, Amund OO (2010) Effects of corn steep liquor on growth rate and pyrene degradation by Pseudomonas strains. Current Microbiol 60:407–411PubMedGoogle Scholar
  59. Obayori OS, Salam LB, Anifowoshe WT, Odunewu ZM, Amosu OE, Ofulue BE (2015) Enhanced Degradation of Petroleum Hydrocarbons in Corn-Steep-Liquor-Treated Soil Microcosm. Soil Sediment Contam 24(7):731–743Google Scholar
  60. Okoh AI (2006) Biodegradation alternative in the clean-up of petroleum hydrocarbon pollutants. Biotechnol Mol Biol Rev 1:38–50Google Scholar
  61. Okolo JC, Amadi EN, Odu CTI (2005) Effect of soil treatments containing poultry manure on crude oil degradation in a sandy loam soil. Appl Ecol Environ Res 3:47–55Google Scholar
  62. Oldenhuis R, Vink RL, Janssen DB, Witholt B (1989) Degradation of chlorinated aliphatic hydrocarbons by Methylosinus trichosporium OB3b expressing soluble methane monooxygenase. Appl Environ Microbiol 55(11):2819–2826PubMedPubMedCentralGoogle Scholar
  63. Oulas A, Pavloudi G, Polymanakou P, Pavlopoulus GA, Papanikolaou N, Kotoulas G, Arvanitidis C, Iliopoulus I (2015) Metagenomics: tools and insights for analyzing next-generation sequencing data derived from biodiversity studies. Bioinform Biol Insights 9:75–88PubMedPubMedCentralGoogle Scholar
  64. Outten FW, Outten CE, O’Halloran T (2000) Metalloregulatory systems at the interface between bacterial metal homeostasis and resistance. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM Press, Washington D.C, pp 145–157Google Scholar
  65. Parks DH, Tyson GW, Hugenhiltz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30(21):3123–3124PubMedPubMedCentralGoogle Scholar
  66. Perez-Pantoja D, De la Iglesia R, Pieper DH, Gonzalez B (2008) Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol Rev 32:736–794Google Scholar
  67. Pérez-Pantoja D, González B, Pieper DH (2010) Aerobic degradation of aromatic hydrocarbons. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 799–837Google Scholar
  68. Perez-Pentoja D, Donoso R, Agullo L, Cordova M, Seeger M, Pieper DH, Gonzalez B (2012) Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol 14(5):1091–1117Google Scholar
  69. Philp JC, Bamforth SM, Singleton I, Atlas RM (2005) Environmental pollution and restoration: a role for bioremediation. In: Atlas RM, Philp J (eds) Applied microbial solutions for real-world environmental clean-up. ASM, Washington, DC, pp 1–48Google Scholar
  70. Pritchard RH, Mueller JG, Rogers JC, Kremer FV, Glaser JA (1992) Oil spill bioremediations: experiences, lesson, and results from the Exxon Valdez oil spill in Alaska. Biodegradation 3:315–335Google Scholar
  71. Rho M, Tang H, Ye Y (2010) FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acid Res 38:20–191Google Scholar
  72. Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11(10):2477–2490PubMedGoogle Scholar
  73. Saha BC, Racine FM (2010) Effect of pH and corn steep liquor variability on mannitol production by Lactobacillus intermidius NRRL B-3693. Appl Microbiol Biotechnol 87:553–556PubMedGoogle Scholar
  74. Salam LB (2016) Metabolism of waste engine oil by Pseudomonas species. 3 Biotech 6(1):1–10Google Scholar
  75. Salam LB, Ilori MO, Amund OO et al (2014) Carbazole angular dioxygenation and mineralization by bacteria isolated from hydrocarbon-contaminated tropical African soil. Environ Sci Pollut Res 21:9311–9324Google Scholar
  76. Salam LB, Ilori MO, Amund OO (2015) Carbazole degradation in the soil microcosm by tropical bacterial strains. Brazilian J Microbiol 46(4):1037–1044Google Scholar
  77. Salam LB, Obayori OS, Nwaokorie FO, Suleiman A, Mustapha R (2017) Metagenomic insights into effects of spent engine oil perturbation on the microbial community composition and function in a tropical agricultural soil. Environ Sci Pollut Res 24:7139–7159Google Scholar
  78. Salam LB, Ilori MO, Amund OO, LiiMien Y, Nojiri H (2018) Characterization of bacterial community structure in a hydrocarbon-contaminated tropical African soil. Environ Technol 39(7):939–951PubMedGoogle Scholar
  79. Schippers A, Bosecker K, Spro¨er C, Schumann P (2005) Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov., novel crude-oil-degrading Gram-positive bacteria. Int J Syst Evol Microbiol 55:655–660PubMedGoogle Scholar
  80. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mother: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541PubMedPubMedCentralGoogle Scholar
  81. Simister R, Poutasse CM, Thurston A, Reeve J, Baker MC, White HK (2015) Degradation of oil by fungi isolated from Gulf of Mexico beaches. Mar Pollut Bull 100(1):327–333PubMedGoogle Scholar
  82. Singer ME, Finnerty WR (1990) Physiology of biosurfactant synthesis by Rhodococcus sp H13-A. Can J Microbiol 36:741–745PubMedGoogle Scholar
  83. Singh V, Pandey VC, Pathak DC, Agrawal S (2012) Purification and characterization of Laceyella sacchari strain B42 xylanase and its potential for pulp biobleaching. Afr J Microbiol Res 6(7):1397–1410Google Scholar
  84. Singleton DR, Dickey AN, Scholl EH, Wright FA, Aitken MD (2016) Complete genome sequence of a bacterium representing a deep uncultivated lineage within the gammaproteobacterial associated with the degradation of polycyclic aromatic hydrocarbons. Genome Announc.  https://doi.org/10.1128/genomeA.01086-16 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143–144:5–22PubMedGoogle Scholar
  86. Spain A, Alm E (2003) Implications of microbial heavy metal tolerance in the environment. Rev Undergraduate Res 2:1–6Google Scholar
  87. Streit WR, Schmitz RA (2004) Metagenomics- key to the uncultured microbes. Curr Opin Microbiol 7:492–498PubMedGoogle Scholar
  88. Tabacchioni S, Chiarini L, Bevivino A et al (2000) Bias caused by using different isolation media for assessing the genetic diversity of a natural microbial population. Microb Ecol 40:169–176PubMedGoogle Scholar
  89. Talfournier F, Stines-Chaumeil C, Branlant G (2011) Methylmalonate semialdehyde dehydrogenase from Bacillus subtilis: substrate specificity and coenzyme a binding. J Biol Chem 286(25):21971–21981PubMedPubMedCentralGoogle Scholar
  90. Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28PubMedPubMedCentralGoogle Scholar
  91. Teal JM, Farrington JW, Burns K, Stegeman J, Tripp BW, Woodin BR, Phinney C (1992) The West Famouth oil spill after 20 years: fate of fuel oil compounds and effects on animals. Marine Pollut Bull 24(12):607–614Google Scholar
  92. Top EM, Springael D (2003) The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol 14:262–269Google Scholar
  93. Trevors JT (1998) Bacterial biodiversity in soil with an emphasis on chemically-contaminated soils. Water Air Soil Pollut 101:45–67Google Scholar
  94. Vasiliou V, Pappa A, Petersen DR (2000) Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem Biol Interact 129:1–19PubMedGoogle Scholar
  95. Villadangos AF, Fu H-L, Gil JA, Messens J, Rosen BP, Meteos LM (2012) Efflux permease CgAcr3-1 of Corynebacterium glutamicum is an arsenite-specific antiporter. J Biol Chem 287(1):723–735PubMedGoogle Scholar
  96. Vivas A, Moreno B, del Val C, Macci C, Masciandaro G, Benitez E (2008) Metabolic and bacterial diversity in soils historically contaminated by heavy metals and hydrocarbons. J Environ Monit 10:1287–1296PubMedGoogle Scholar
  97. Yakubu MB (2007) Biodegradation of Lagoma crude oil using pig dung. Afr J Biotechnol 6(24):2821–2825Google Scholar
  98. Yveline LD, Frederick J, Pierre D, Michael G, Jean CB, Gilbert M (1997) Hydrocarbon balance of a site which had been highly and chronically contaminated by petroleum wastes of refinery from 1956 to 1997. Marine Pollut Bull 22:103–109Google Scholar
  99. Zabielska-Matejuk J, Czaczyk K (2006) Biodegradation of newquartenaey ammonium compounds in treated wood by mould fungi. Wood Sci Technol 40(6):461–475Google Scholar
  100. Zhang D-C, Schinner F, Margesin R (2010a) Pedobacter bauzanensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:2592–2595PubMedGoogle Scholar
  101. Zhang J, Tang S-K, Zhang Y-Q, Yu L-Y, Klenk H-P, Li W-J (2010b) Laceyella tengchongensis sp. nov., a thermophile isolated from soil of a volcano. Int J Syst Evol Microbiol 60:2226–2230PubMedGoogle Scholar
  102. Zhang D-C. Liu H-C, Zhou Y-G, Schinner F, Mrgesin R (2011) Pseudomonas bauzanensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 61:2333–2337PubMedGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesMicrobiology Unit Al-Hikmah UniversityIlorinNigeria

Personalised recommendations