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http://dx.doi.org/10.4014/jmb.2104.04023

Biodegradation and Removal of PAHs by Bacillus velezensis Isolated from Fermented Food  

Sultana, Omme Fatema (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University)
Lee, Saebim (Probiotics Microbiome Convergence Center, Soonchunhyang University)
Seo, Hoonhee (Probiotics Microbiome Convergence Center, Soonchunhyang University)
Al Mahmud, Hafij (Probiotics Microbiome Convergence Center, Soonchunhyang University)
Kim, Sukyung (Probiotics Microbiome Convergence Center, Soonchunhyang University)
Seo, Ahyoung (Probiotics Microbiome Convergence Center, Soonchunhyang University)
Kim, Mijung (Probiotics Microbiome Convergence Center, Soonchunhyang University)
Song, Ho-Yeon (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University)
Publication Information
Journal of Microbiology and Biotechnology / v.31, no.7, 2021 , pp. 999-1010 More about this Journal
Abstract
Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous in the environment. They are highly toxigenic and carcinogenic. Probiotic bacteria isolated from fermented foods were tested to check their ability to degrade and/or detoxify PAHs. Five probiotic bacteria with distinct morphologies were isolated from a mixture of 26 fermented foods co-cultured with benzo(a)pyrene (BaP) containing Bushnell Haas minimal broth. Among them, B. velezensis (PMC10) significantly reduced the abundance of BaP in the broth. PMC10 completely degraded BaP presented at a lower concentration in broth culture. B. velezensis also showed a clear zone of degradation on a BaP-coated Bushnell Haas agar plate. Gene expression profiling showed significant increases of PAH ring-hydroxylating dioxygenases and 4-hydroxybenzoate 3-monooxygenase genes in B. velezensis in response to BaP treatment. In addtion, both live and heat-killed B. velezensis removed BaP and naphthalene (Nap) from phosphate buffer solution. Live B. velezensis did not show any cytotoxicity to macrophage or human dermal fibroblast cells. Live-cell and cell-free supernatant of B. velezensis showed potential anti-inflammatory effects. Cell-free supernatant and extract of B. velezensis also showed free radical scavenging effects. These results highlight the prospective ability of B. velezensis to biodegrade and remove toxic PAHs from the human body and suggest that the biodegradation of BaP might be regulated by ring-hydroxylating dioxygenase-initiated metabolic pathway.
Keywords
PAH degradation; PAH removal; B. velezensis; fermented food; probiotics; ring-hydroxylating dioxygenase;
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1 Diggs DL, Huderson AC, Harris KL, Myers JN, Banks LD, Rekhadevi P V, et al. 2011. Polycyclic aromatic hydrocarbons and digestive tract cancers: a perspective. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 29: 324-357.   DOI
2 Poursafa P, Moosazadeh M, Abedini E, Hajizadeh Y, Mansourian M, Pourzamani H, et al. 2017. A systematic review on the effects of polycyclic aromatic hydrocarbons on cardiometabolic impairment. Int. J. Prev. Med. 8: 19.   DOI
3 Fijan S. 2014. Microorganisms with claimed probiotic properties: an overview of recent literature. Int. J. Environ. Res. Public Health 11: 4745-4767.   DOI
4 Yun SH, Choi C-W, Lee S-Y, Lee YG, Kwon J, Leem SH, et al. 2014. Proteomic characterization of plasmid pLA1 for biodegradation of polycyclic aromatic hydrocarbons in the marine bacterium, Novosphingobium pentaromativorans US6-1. PLoS One 9: e90812.   DOI
5 Sangsila A, Faucet-Marquis V, Pfohl-Leszkowicz A, Itsaranuwat P. 2016. Detoxification of zearalenone by Lactobacillus pentosus strains. Food Control 62: 187-192.   DOI
6 Mahmud HA, Seo H, Kim S, Islam MI, Nam K-W, Cho H-D, et al. 2017. Thymoquinone (TQ) inhibits the replication of intracellular Mycobacterium tuberculosis in macrophages and modulates nitric oxide production. BMC Complement. Altern. Med. 17: 1-8.   DOI
7 Kim M, Chun J. 2014. 16S rRNA gene-based identification of bacteria and archaea using the EzTaxon server. Methods Microbiol. 41: 61-74.   DOI
8 Siddens LK, Larkin A, Krueger SK, Bradfield CA, Waters KM, Tilton SC, et al. 2012. Polycyclic aromatic hydrocarbons as skin carcinogens: comparison of benzo [a] pyrene, dibenzo [def, p] chrysene and three environmental mixtures in the FVB/N mouse. Toxicol. Appl. Pharmacol. 264: 377-386.   DOI
9 Program NT. 2000. Toxicology and carcinogenesis studies of naphthalene in F344/N rats. US Dep. Heal. Hum. Serv. Natl. Toxicol. Program, Washington, DC ., USA.
10 Dominici L, Villarini M, Trotta F, Federici E, Cenci G, Moretti M. 2014. Protective effects of probiotic Lactobacillus rhamnosus IMC501 in mice treated with PhIP. J. Microbiol. Biotechnol. 24: 371-378.   DOI
11 Rafter J. 2004. The effects of probiotics on colon cancer development. Nutr. Res. Rev. 17: 277-284.   DOI
12 Boffetta P, Jourenkova N, Gustavsson P. 1997. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control 8: 444-472.   DOI
13 Karimi B, Habibi M, Esvand M. 2015. Biodegradation of naphthalene using Pseudomonas aeruginosa by up flow anoxic-aerobic continuous flow combined bioreactor. J. Environ. Health Sci. Eng. 13: 26.   DOI
14 Lyu Y, Zheng W, Zheng T, Tian Y. 2014. Biodegradation of polycyclic aromatic hydrocarbons by Novosphingobium pentaromativorans US6-1. PLoS One 9: e101438.   DOI
15 Bogardt AH, Hemmingsen BB. 1992. Enumeration of phenanthrene-degrading bacteria by an overlayer technique and its use in evaluation of petroleum-contaminated sites. Appl. Environ. Microbiol. 58: 2579-2582.   DOI
16 Oyehan TA, Al-Thukair AA. 2017. Isolation and characterization of PAH-degrading bacteria from the Eastern Province, Saudi Arabia. Mar. Pollut. Bull. 115: 39-46.   DOI
17 Sarlak Z, Rouhi M, Mohammadi R, Khaksar R, Mortazavian AM, Sohrabvandi S, et al. 2017. Probiotic biological strategies to decontaminate aflatoxin M1 in a traditional Iranian fermented milk drink (Doogh). Food Control 71:152-159.   DOI
18 Petti CA. 2008. Interpretive criteria for identification of bacteria and fungi by DNA target sequencing. Clinical and Laboratory Standards Institute.
19 Shen Q, Shang N, Li P. 2011. In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr. Microbiol. 62: 1097-1103.   DOI
20 Janda JM, Abbott SL. 2007. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J. Clin. Microbiol. 45: 2761-2764.   DOI
21 Mahmud H Al, Seo H, Kim S, Islam MI, Nam K-W, Cho H-D, et al. 2017. Thymoquinone (TQ) inhibits the replication of intracellular Mycobacterium tuberculosis in macrophages and modulates nitric oxide production. BMC Complement. Altern. Med. 17: 279.   DOI
22 Nimse SB, Pal D. 2015. Free radicals, natural antioxidants, and their reaction mechanisms. Rsc. Adv. 5: 27986-28006.   DOI
23 Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J. 2015. Probiotics as potential antioxidants: a systematic review. J. Agric. Food Chem. 63: 3615-3626.   DOI
24 El-Nawawy MA, El-Malkey W, Aumara IE. 2009. Production and properties of antioxidative fermented probiotic beverages with natural fruit juices. Ann. Agric. Sci. 54: 121-135.
25 Grady EN, MacDonald J, Ho MT, Weselowski B, McDowell T, Solomon O, et al. 2019. Characterization and complete genome analysis of the surfactin-producing, plant-protecting bacterium Bacillus velezensis 9D-6. BMC Microbiol. 19: 5.   DOI
26 Ismail A, Levin RE, Riaz M, Akhtar S, Gong YY, de Oliveira CAF. 2017. Effect of different microbial concentrations on binding of aflatoxin M1 and stability testing. Food Control 73: 492-496.   DOI
27 Silva F de J, Ferreira LC, Campos VP, Cruz-Magalhaes V, Barros AF, Andrade JP, et al. 2019. Complete genome sequence of the biocontrol agent Bacillus velezensis UFLA258 and its comparison with related species: diversity within the commons. Genome Biol. Evol. 11: 2818-2823.   DOI
28 Choi J, Nam J, Seo M-H. 2021. Complete genome sequence of Bacillus velezensis NST6 and comparison with the species belonging to operational group B. amyloliquefaciens. Genomics 113: 380-386.   DOI
29 De Marco S, Sichetti M, Muradyan D, Piccioni M, Traina G, Pagiotti R, et al. 2018. Probiotic cell-free supernatants exhibited antiinflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid. Based Complement. Altern. Med. 2018: 1756308.   DOI
30 Samanta SK, Singh O V, Jain RK. 2002. Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol. 20: 243-248.   DOI
31 Liu H, Zeng Q, Wang W, Zhang R, Yao J. 2020. Complete genome sequence of Bacillus velezensis strain AL7, a biocontrol agent for suppression of cotton Verticillium wilt. Microbiol. Resour. Announc. 9: e015959-19.
32 Kim S, Seo H, Mahmud H Al, Islam MI, Sultana OF, Lee Y, et al. 2020. Melanin Bleaching and melanogenesis inhibition effects of Pediococcus acidilactici PMC48 isolated from Korean Perilla Leaf Kimchi. J. Microbiol. Biotechnol. 30: 1051-1059.   DOI
33 Haritash AK, Kaushik CP. 2009. Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J. Hazard Mater. 169: 1-15.   DOI
34 Sowada J, Schmalenberger A, Ebner I, Luch A, Tralau T. 2014. Degradation of benzo [a] pyrene by bacterial isolates from human skin. FEMS Microbiol. Ecol. 88: 129-139.   DOI
35 Yousefi M, Shariatifar N, Tajabadi Ebrahimi M, Mortazavian AM, Mohammadi A, Khorshidian N, et al. 2019. In vitro removal of polycyclic aromatic hydrocarbons by lactic acid bacteria. J. Appl. Microbiol. 126: 954-964.   DOI
36 Okai M, Kihara I, Yokoyama Y, Ishida M, Urano N. 2015. Isolation and characterization of benzo [a] pyrene-degrading bacteria from the Tokyo Bay area and Tama River in Japan. FEMS Microbiol. Lett. 362: fnv143.   DOI
37 Kim K-H, Jahan SA, Kabir E, Brown RJC. 2013. A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ. Int. 60: 71-80.   DOI
38 Karami S, Boffetta P, Brennan P, Stewart PA, Zaridze D, Matveev V, et al. 2011. Renal cancer risk and occupational exposure to polycyclic aromatic hydrocarbons and plastics. J. Occup. Environ. Med. 53: 218-223.   DOI
39 Abdel-Shafy HI, Mansour MSM. 2016. A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J. Pet. 25: 107-123.   DOI
40 Kechagia M, Basoulis D, Konstantopoulou S, Dimitriadi D, Gyftopoulou K, Skarmoutsou N, et al. 2013. Health benefits of probiotics: a review. ISRN Nutr. 2013: 481651.   DOI
41 Aubin GG, Bemer P, Kambarev S, Patel NB, Lemenand O, Caillon J, et al. 2016. Propionibacteriumnamnetense sp. nov., isolated from a human bone infection. Int. J. Syst. Evol. Microbiol. 66: 3393-3399.   DOI
42 Rajendran R, Ohta Y. 1998. Binding of heterocyclic amines by lactic acid bacteria from miso, a fermented Japanese food. Can J. Microbiol. 44: 109-115.   DOI
43 Abou-Arab AAK, Abou-Bakr S, Maher RA, El-Hendawy HH, Awad AA. 2015. Persistence of some lactic acid bacteria as affected by polycyclic aromatic hydrocarbons. J. Microbiol. Exp. 2: 1-6.
44 Abou-Arab AAK, Salim A-B, Maher RA, El-Hendawy HH, Awad AA. 2010. Degradation of polycyclic aromatic hydrocarbons as affected by some lactic acid bacteria. J. Am. Sci. 6: 1237-1246.
45 Tatusov RL, Galperin MY, Natale DA, Koonin E V. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28: 33-36.   DOI
46 Lee I, Kim YO, Park S-C, Chun J. 2016. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 66: 1100-1103.   DOI