1887

Access Microbiology open research platform logo

Volume 5, Issue 6

Bacterial community dynamics and associated genes in hydrocarbon contaminated soil during bioremediation using brewery spent grain Open Access

Abstract

Brewery spent grain (BSG) has previously been exploited in bioremediation. However, detailed knowledge of the associated bacterial community dynamics and changes in relevant metabolites and genes over time is limited. This study investigated the bioremediation of diesel contaminated soil amended with BSG. We observed complete degradation of three total petroleum hydrocarbon (TPH C10–C28) fractions in amended treatments as compared to one fraction in the unamended, natural attenuation treatments. The biodegradation rate constant () was higher in amended treatments (0.1021) than in unamended (0.059), and bacterial colony forming units increased significantly in amended treatments. The degradation compounds observed fitted into the elucidated diesel degradation pathways and quantitative PCR results showed that the gene copy numbers of all three associated degradation genes, , and were significantly higher in amended treatments. High-throughput sequencing of 16S rRNA gene amplicons showed that amendment with BSG enriched autochthonous hydrocarbon degraders. Also, community shifts of the genera and correlated with the abundance of catabolic genes and degradation compounds observed. This study showed that these two genera are present in BSG and thus may be associated with the enhanced biodegradation observed in amended treatments. The results suggest that the combined evaluation of TPH, microbiological, metabolite and genetic analysis provides a useful holistic approach to assessing bioremediation.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): alkB, catA, xylE catabolic genes , bacterial community profiling , bioremediation , brewery spent grain , diesel metabolites and total petroleum hydrocarbons
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000519.v3
2023-06-20
2024-05-05
Loading full text...

Full text loading...

/deliver/fulltext/acmi/5/6/acmi000519.v3.html?itemId=/content/journal/acmi/10.1099/acmi.0.000519.v3&mimeType=html&fmt=ahah

References

  1. Aziz S, Ali MI, Farooq U, Jamal A, Liu F-J et al. Enhanced bioremediation of diesel range hydrocarbons in soil using biochar made from organic wastes. Environ Monit Assess 2020; 192: [View Article]
     [Google Scholar]
  2. Tellechea FR, Martins MA, Silva AO, Netto AF, Martins ML. Ex situ bioremediation of a tropical soil contaminated with diesel. JSM Biol 2017; 2:1
     [Google Scholar]
  3. Yergeau E, Sanschagrin S, Beaumier D, Greer CW. Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS One 2012; 7:e30058 [View Article] [PubMed]
     [Google Scholar]
  4. Souza EC, Vessoni-Penna TC, de Souza Oliveira RP. Biosurfactant-enhanced hydrocarbon bioremediation: an overview. Int Biodeterior Biodegrad 2014; 89:88–94 [View Article]
     [Google Scholar]
  5. Varjani SJ. Microbial degradation of petroleum hydrocarbons. Bioresour Technol 2017; 223:277–286 [View Article] [PubMed]
     [Google Scholar]
  6. Semple KT, Reid BJ, Fermor TR. Impact of composting strategies on the treatment of soils contaminated with organic pollutants. Environ Pollut 2001; 112:269–283 [View Article] [PubMed]
     [Google Scholar]
  7. Truskewycz A, Gundry TD, Khudur LS, Kolobaric A, Taha M et al. Petroleum Hydrocarbon Contamination in Terrestrial Ecosystems-Fate and Microbial Responses. Molecules 2019; 24:3400 [View Article] [PubMed]
     [Google Scholar]
  8. Gao Y-C, Guo S-H, Wang J-N, Li D, Wang H et al. Effects of different remediation treatments on crude oil contaminated saline soil. Chemosphere 2014; 117:486–493 [View Article] [PubMed]
     [Google Scholar]
  9. Jansson JK, Hofmockel KS. The soil microbiome-from metagenomics to metaphenomics. Curr Opin Microbiol 2018; 43:162–168 [View Article] [PubMed]
     [Google Scholar]
  10. Wyszkowski M, Wyszkowska J, Borowik A, Kordala N. Contamination of soil with diesel oil, application of sewage sludge and content of macroelements in oats. Water Air Soil Pollut 2020; 231: [View Article]
     [Google Scholar]
  11. Shahsavari E, Adetutu EM, Anderson PA, Ball AS. Plant residues — A low cost, effective bioremediation treatment for petrogenic hydrocarbon-contaminated soil. Sci Total Environ 2013; 443:766–774 [View Article]
     [Google Scholar]
  12. Sarkar J, Kazy SK, Gupta A, Dutta A, Mohapatra B et al. Biostimulation of indigenous microbial community for bioremediation of petroleum refinery sludge. Front Microbiol 2016; 7:1407 [View Article] [PubMed]
     [Google Scholar]
  13. Guarino C, Spada V, Sciarrillo R. Assessment of three approaches of bioremediation (Natural Attenuation, Landfarming and Bioagumentation - Assistited Landfarming) for a petroleum hydrocarbons contaminated soil. Chemosphere 2017; 170:10–16 [View Article] [PubMed]
     [Google Scholar]
  14. Bekele GK, Gebrie SA, Mekonen E, Fida TT, Woldesemayat AA et al. Isolation and characterization of diesel-degrading bacteria from hydrocarbon-contaminated sites, flower farms, and soda lakes. Int J Microbiol 2022; 2022:5655767 [View Article] [PubMed]
     [Google Scholar]
  15. Das N, Chandran P. Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int 2011; 2011:941810 [View Article] [PubMed]
     [Google Scholar]
  16. Eze MO, Thiel V, Hose GC, George SC, Daniel R. Bacteria-plant interactions synergistically enhance biodegradation of diesel fuel hydrocarbons. Commun Earth Environ 2022; 3:192 [View Article]
     [Google Scholar]
  17. Sheppard PJ, Adetutu EM, Makadia TH, Ball AS. Microbial community and ecotoxicity analysis of bioremediated, weathered hydrocarbon-contaminated soil. Soil Res 2011; 49:261 [View Article]
     [Google Scholar]
  18. Fuentes S, Méndez V, Aguila P, Seeger M. Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 2014; 98:4781–4794 [View Article] [PubMed]
     [Google Scholar]
  19. Wu M, Guo X, Wu J, Chen K. Effect of compost amendment and bioaugmentation on PAH degradation and microbial community shifting in petroleum-contaminated soil. Chemosphere 2020; 256:126998 [View Article] [PubMed]
     [Google Scholar]
  20. Lima-Morales D, Jáuregui R, Camarinha-Silva A, Geffers R, Pieper DH et al. Linking microbial community and catabolic gene structures during the adaptation of three contaminated soils under continuous long-term pollutant stress. Appl Environ Microbiol 2016; 82:2227–2237 [View Article] [PubMed]
     [Google Scholar]
  21. Yang Y, Wang J, Liao J, Xie S, Huang Y. Abundance and diversity of soil petroleum hydrocarbon-degrading microbial communities in oil exploring areas. Appl Microbiol Biotechnol 2015; 99:1935–1946 [View Article]
     [Google Scholar]
  22. Garrido-Sanz D, Redondo-Nieto M, Guirado M, Pindado Jiménez O, Millán R et al. Metagenomic insights into the bacterial functions of a diesel-degrading consortium for the rhizoremediation of diesel-polluted soil. Genes 2019; 10:456 [View Article] [PubMed]
     [Google Scholar]
  23. Gielnik A, Pechaud Y, Huguenot D, Cébron A, Esposito G et al. Bacterial seeding potential of digestate in bioremediation of diesel contaminated soil. IBB 2019; 143:104715 [View Article]
     [Google Scholar]
  24. Kawagoe T, Kubota K, Araki KS, Kubo M. Analysis of the alkane hydroxylase gene and long-chain cyclic alkane degradation in Rhodococcus . Adv Microbiol 2019; 9: [View Article]
     [Google Scholar]
  25. Kulshreshtha S. Current trends in bioremediation and biodegradation. J Bioremed Biodegrad 2012; 03: [View Article]
     [Google Scholar]
  26. Umar ZD, Aziz NA, Zulkiflia SZ, Mustafa M. Rapid biodegradation of polycyclic aromatic hydrocarbons (pahs). MethodsX 2017 [View Article]
     [Google Scholar]
  27. Yanto DHY, Tachibana S. Biodegradation of petroleum hydrocarbons by a newly isolated Pestalotiopsis sp. NG007. Int Biodeterior Biodegrad 2013; 85:438–450 [View Article]
     [Google Scholar]
  28. Wu M, Dick WA, Li W, Wang X, Yang Q et al. Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. Inter Biodeter Biodegr 2016 [View Article]
     [Google Scholar]
  29. Zucchi M, Angiolini L, Borin S, Brusetti L, Dietrich N et al. Response of bacterial community during bioremediation of an oil-polluted soil*. J Appl Microbiol 2003; 94:248–257 [View Article] [PubMed]
     [Google Scholar]
  30. Reddy MV, Devi MP, Chandrasekhar K, Goud RK, Mohan SV. Aerobic remediation of petroleum sludge through soil supplementation: microbial community analysis. J Hazard Mat 2011; 197:80–87 [View Article]
     [Google Scholar]
  31. Chandra S, Sharma R, Singh K, Sharma A. Application of bioremediation technology in the environment contaminated with petroleum hydrocarbon. Ann Microbiol 2013; 63:417–431 [View Article]
     [Google Scholar]
  32. Dussán J, Numpaque M. Degradation of diesel, a component of the explosive ANFO, by bacteria selected from an open cast coal mine in La Guajira, Colombia. J Bioproces Biotechniq 2012; 02: [View Article]
     [Google Scholar]
  33. Agamuthu P, Tan YS, Fauziah SH. Bioremediation of hydrocarbon contaminated soil using selected organic wastes. Procedia Environ Sci 2013; 18:694–702 [View Article]
     [Google Scholar]
  34. Lynch KM, Steffen EJ, Arendt EK. Brewers’ spent grain: a review with an emphasis on food and health. J Inst Brew 2016; 122:553–568 [View Article]
     [Google Scholar]
  35. Thomas KR, Rahman P. Brewery wastes. strategies for sustainability. A review. Aspects Appl Biol 2006; 80:
     [Google Scholar]
  36. Agarry S, Latinwo KG. Biodegradation of diesel oil in soil and its enhancement by application of bioventing and amendment with brewery waste effluents as biostimulation - bioaugmentation agents. J Ecol Eng 2015; 16:82–91 [View Article]
     [Google Scholar]
  37. Abioye OP, Agamuthu P, Abdul Aziz AR. Biodegradation of used motor oil in soil using organic waste amendments. Biotechnol Res Int 2012; 2012:587041 [View Article] [PubMed]
     [Google Scholar]
  38. Agamuthu P, Abioye OP, Aziz AA. Phytoremediation of soil contaminated with used lubricating oil using Jatropha curcas. J Hazard Mater 2010; 179:891–894 [View Article] [PubMed]
     [Google Scholar]
  39. Robertson JA, I’Anson KJA, Treimo J, Faulds CB, Brocklehurst TF et al. Profiling brewers’ spent grain for composition and microbial ecology at the site of production. LWT - Food Sc Technol 2010; 43:890–896 [View Article]
     [Google Scholar]
  40. Bianco A, Budroni M, Zara S, Mannazzu I, Fancello F et al. The role of microorganisms on biotransformation of brewers’ spent grain. Appl Microbiol Biotechnol 2020; 104:8661–8678 [View Article]
     [Google Scholar]
  41. Emmett B, Reynolds B, Chamberlain P, Rowe E, Spurgeon D et al. Countryside survey: Soils report from 2007. In Centre for Ecology and Hydrology Oxon UK: Wallingford; 2010
     [Google Scholar]
  42. Fernández MD, Pro J, Alonso C, Aragonese P, Tarazona JV. Terrestrial microcosms in a feasibility study on the remediation of diesel-contaminated soils. Ecotoxicol Environ Saf 2011; 74:2133–2140 [View Article] [PubMed]
     [Google Scholar]
  43. Emam TM, Espeland EK, Rinella MJ. Soil sterilization alters interactions between the native grass Bouteloua gracilis and invasive Bromus tectorum . J Arid Environ 2014; 111:91–97 [View Article]
     [Google Scholar]
  44. Molina-Barahona L, Rodrı́guez-Vázquez R, Hernández-Velasco M, Vega-Jarquı́n C, Zapata-Pérez O et al. Diesel removal from contaminated soils by biostimulation and supplementation with crop residues. Appl Soil Ecol 2004; 27:165–175 [View Article]
     [Google Scholar]
  45. Chagas-Spinelli ACO, Kato MT, de Lima ES, Gavazza S. Bioremediation of a tropical clay soil contaminated with diesel oil. J Environ Manag 2012; 113:510–516 [View Article]
     [Google Scholar]
  46. Bento FM, Camargo FAO, Okeke BC, Frankenberger WT. Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresource Technol 2005; 96:1049–1055 [View Article]
     [Google Scholar]
  47. Suja F, Rahim F, Taha MR, Hambali N, Rizal Razali M et al. Effects of local microbial bioaugmentation and biostimulation on the bioremediation of total petroleum hydrocarbons (TPH) in crude oil contaminated soil based on laboratory and field observations. IBB 2014; 90:115–122 [View Article]
     [Google Scholar]
  48. Baek KH, Kim H, Moon S, Lee I, Oh H et al. Effects of soil types on the biodegradation of crude oil by nocardia sp H17. J Microbiol Biotechnol 2004; 15,901:
     [Google Scholar]
  49. Xu Y, Lu M. Bioremediation of crude oil-contaminated soil: comparison of different biostimulation and bioaugmentation treatments. J Hazard Materials 2010; 183:395–401 [View Article]
     [Google Scholar]
  50. Dineen SM, Aranda IVR, Anders DL, Robertson JM. An evaluation of commercial DNA extraction kits for the isolation of bacterial spore DNA from soil. J Appl Microbiol 2010; 109:1886–1896 [View Article]
     [Google Scholar]
  51. Powell SM, Ferguson SH, Bowman JP, Snape IS. Using real-time PCR to assess changes in the hydrocarbon-degrading microbial community in Antarctic soil during bioremediation. Microb Ecol 2006; 52:523–532 [View Article] [PubMed]
     [Google Scholar]
  52. Shahsavari E, Aburto-Medina A, Taha M, Ball AS. A quantitative PCR approach for quantification of functional genes involved in the degradation of polycyclic aromatic hydrocarbons in contaminated soils. MethodsX 2016; 3:205–211 [View Article] [PubMed]
     [Google Scholar]
  53. Nnadi MO. Bacterial community dynamics during the bioremediation of diesel contaminated soil using brewery spent grain. Dissertation University of Sunderland; 2019
     [Google Scholar]
  54. Staroscik A. ds DNA copy number calculator; 2004 http://cels.uri.edu/gsc/cndna.html accessed 27 June 2022
  55. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 2011; 108 Suppl 1:4516–4522 [View Article] [PubMed]
     [Google Scholar]
  56. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72:5069–5072 [View Article] [PubMed]
     [Google Scholar]
  57. Chikere CB, Surridge KJ, Cloete ET, Okpokwasili GC. Phylogenetic diversity of dominant bacterial communities during bioremediation of crude oil-polluted soil. Ambi-Agua 2011; 6:61–76 [View Article]
     [Google Scholar]
  58. van Elsas JD, Trevors JT, Jansson JK, Nannipieri P. Modern Soil Microbiology New York: CRC Press; 2007 pp 387–429 [View Article]
     [Google Scholar]
  59. Margesin R, Labbé D, Schinner F, Greer CW, Whyte LG. Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine Alpine soils. Appl Environ Microbiol 2003; 69:3085–3092 [View Article] [PubMed]
     [Google Scholar]
  60. Alisi C, Musella R, Tasso F, Ubaldi C, Manzo S et al. Bioremediation of diesel oil in a co-contaminated soil by bioaugmentation with a microbial formula tailored with native strains selected for heavy metals resistance. Sci Total Environ 2009; 407:3024–3032 [View Article] [PubMed]
     [Google Scholar]
  61. Karamalidis AK, Evangelou AC, Karabika E, Koukkou AI, Drainas C et al. Laboratory scale bioremediation of petroleum-contaminated soil by indigenous microorganisms and added Pseudomonas aeruginosa strain Spet. Bioresour Technol 2010; 101:6545–6552 [View Article] [PubMed]
     [Google Scholar]
  62. Ros M, Rodríguez I, García C, Hernández T. Microbial communities involved in the bioremediation of an aged recalcitrant hydrocarbon polluted soil by using organic amendments. Bioresource Technol 2010; 101:6916–6923 [View Article]
     [Google Scholar]
  63. Varjani SJ, Upasani VN. A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. IBB 2017; 120:71–83 [View Article]
     [Google Scholar]
  64. Kingston PF. Long-term environmental impact of oil spills. Spill Sci Technol Bull 2002; 7:53–61 [View Article]
     [Google Scholar]
  65. Margesin R, Moertelmaier C, Mair J. Low-temperature biodegradation of petroleum hydrocarbons (n-alkanes, phenol, anthracene, pyrene) by four actinobacterial strains. Int Biodeter Biodegr 2013; 84:185–191 [View Article]
     [Google Scholar]
  66. Schwarz A, Adetutu EM, Juhasz AL, Aburto-Medina A, Ball AS et al. Microbial degradation of phenanthrene in pristine and contaminated sandy soils. Microb Ecol 2018; 75:888–902 [View Article] [PubMed]
     [Google Scholar]
  67. Eze MO. Metagenome analysis of a hydrocarbon-degrading bacterial consortium reveals the specific roles of BTEX biodegraders. Genes 2021; 12:98 [View Article]
     [Google Scholar]
  68. Olajire AA EJ. Aerobic degradation of petroleum components by microbial consortia. J Pet Environ Biotechnol 2014; 05: [View Article]
     [Google Scholar]
  69. Okoh IA. Biodegradation alternative in the cleanup of petroleum hydrocarbon pollutants. Biotechnol Mol Biol Rev 2006; 1:38–50
     [Google Scholar]
  70. Tsugawa H, Tsujimoto Y, Arita M, Bamba T, Fukusaki E. GC/MS based metabolomics: development of a data mining system for metabolite identification by using soft independent modeling of class analogy (SIMCA). BMC Bioinformatics 2011; 12:131 [View Article] [PubMed]
     [Google Scholar]
  71. Fuchs G, Boll M, Heider J. Microbial degradation of aromatic compounds - from one strategy to four. Nat Rev Microbiol 2011; 9:803–816 [View Article] [PubMed]
     [Google Scholar]
  72. Ghosal D, Ghosh S, Dutta TK, Ahn Y. Corrigendum: current state of knowledge in microbial degradation of Polycyclic Aromatic Hydrocarbons (PAHs): a review. Front Microbiol 2016; 7:1837 [View Article] [PubMed]
     [Google Scholar]
  73. Rojo F. Degradation of alkanes by bacteria. Environ Microbiol 2009; 11:2477–2490 [View Article] [PubMed]
     [Google Scholar]
  74. Wang W, Wang L, Shao Z. Diversity and abundance of oil-degrading bacteria and alkane hydroxylase (alkB) genes in the subtropical seawater of Xiamen Island. Microb Ecol 2010; 60:429–439 [View Article] [PubMed]
     [Google Scholar]
  75. Marcus A. Versatile soil-dwelling microbe is mapped; 2003 http://www.genomenewsnetwork.org/articles/01_03/soil_microbe.shtml accessed 27 June 2022
  76. Harwood CS, Parales RE. The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 1996; 50:553–590 [View Article] [PubMed]
     [Google Scholar]
  77. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H et al. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 2002; 4:799–808 [View Article] [PubMed]
     [Google Scholar]
  78. Méndez V, Fuentes S, Hernández M, Morgante V, González M et al. Isolation of hydrocarbon-degrading heavy-metal-resistant bacteria from crude oil-contaminated soil in central chile. J Biotechnol 2010; 150:287 [View Article]
     [Google Scholar]
  79. Zhang X-X, Cheng S-P, Zhu C-J, Sun S-L. Microbial PAH-degradation in soil: degradation pathways and contributing factors. Pedosphere 2006; 16:555–565 [View Article]
     [Google Scholar]
  80. Naether A, Foesel BU, Naegele V, Wüst PK, Weinert J et al. Environmental factors affect Acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 2012; 78:7398–7406 [View Article] [PubMed]
     [Google Scholar]
  81. Sei K, Asano K, Tateishi N, Mori K, Ike M et al. Design of PCR primers and gene probes for the general detection of bacterial populations capable of degrading aromatic compounds via catechol cleavage pathways. J Biosci Bioeng 1999; 88:542–550 [View Article] [PubMed]
     [Google Scholar]
  82. El Azhari N, Devers-Lamrani M, Chatagnier G, Rouard N, Martin-Laurent F. Molecular analysis of the catechol-degrading bacterial community in a coal wasteland heavily contaminated with PAHs. J Hazard Mater 2010; 177:593–601 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/acmi/10.1099/acmi.0.000519.v3
Loading
Bacterial community dynamics and associated genes in hydrocarbon contaminated soil during bioremediation using brewery spent grain
Access Microbiology 5, 000519.v3 (2023); https://doi.org/10.1099/acmi.0.000519.v3
/content/journal/acmi/10.1099/acmi.0.000519.v3
/content/journal/acmi/10.1099/acmi.0.000519.v3
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error