Differences in the bacteriome of smokeless tobacco products with different oral carcinogenicity: Compositional and predicted functional analysis

Genes

Volumn 8, Issue 4, 2017, Pages

  Al Hebshi, Nezar Noor ^a,b   Ali Alharbi, Fahd ^a   Mahri, Mohammed ^a   Chen, Tsute ^c  

^a JAZAN UNIVERSITY   (Saudi Arabia)

^b TEMPLE UNIVERSITY   (United States)

^c FORSYTH INSTITUTE   (United States)

Author keywords

Bacteria; Bacteriome; Carcinoma; Microbiome; Mouth; Smokeless; Snuff; Tobacco

Indexed keywords

CADMIUM; NICKEL; RNA 16S;

ARTICLE; BACILLUS; BACTERIAL GENE; BACTERIAL LOAD; BACTERIAL MICROBIOME; CARCINOGENICITY; CONTROLLED STUDY; LYSINIBACILLUS; NEXT GENERATION SEQUENCING; NONHUMAN; PAENIBACILLUS; PHYLOGENY; PROPIONIBACTERIUM; PSEUDOMONAS; REAL TIME POLYMERASE CHAIN REACTION; SMOKELESS TOBACCO; SPECIES DIVERSITY; SPECIES RICHNESS; SWEDISH SNUS; YEMENI SHAMMAH;

EID: 85016157244     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes8040106     Document Type: Article

References (50)

1. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans; International Agency for Research on Cancer. Smokeless tobacco and some tobacco-specific N-nitrosamines. In A Review of Human Carcinogens: Personal Habits and Indoor Combustions, Volume 100 E; World Health Organization; distributed by WHO Press: Lyon, France; Geneva, Switzerland, 2012; pp. 267–321.
2. Lee, P.N.; Hamling, J. Systematic review of the relation between smokeless tobacco and cancer in Europe and North America. BMC Med. 2009, 7, 36. [CrossRef] [PubMed]
3. Rodu, B.; Jansson, C. Smokeless tobacco and oral cancer: A review of the risks and determinants. Crit Rev. Oral Biol. Med. 2004, 15, 252–263. [CrossRef] [PubMed]
4. Weitkunat, R.; Sanders, E.; Lee, P.N. Meta-analysis of the relation between European and American smokeless tobacco and oral cancer. BMC Public Health 2007, 7, 334. [CrossRef] [PubMed]
5. Elbeshir, E.I.; Abeen, H.A.; Idris, A.M.; Abbas, K. Snuff dipping and oral cancer in Sudan: A retrospective study. Br. J. Oral Maxillofac. Surg. 1989, 27, 243–248. [PubMed]
6. Idris, A.M.; Ahmed, H.M.; Malik, M.O. Toombak dipping and cancer of the oral cavity in the Sudan: A case-control study. Int J. Cancer 1995, 63, 477–480. [CrossRef] [PubMed]
7. Idris, A.M.; Ahmed, H.M.; Mukhtar, B.I.; Gadir, A.F.; el-Beshir, E.I. Descriptive epidemiology of oral neoplasms in Sudan 1970-1985 and the role of toombak. Int J. Cancer 1995, 61, 155–158. [CrossRef] [PubMed]
8. Allard, W.F.; DeVol, E.B.; Te, O.B. Smokeless tobacco (shamma) and oral cancer in Saudi Arabia. Community Dent. Oral Epidemiol. 1999, 27, 398–405. [CrossRef] [PubMed]
9. Scheifele, C.; Nassar, A.; Reichart, P.A. Prevalence of oral cancer and potentially malignant lesions among shammah users in Yemen. Oral Oncol. 2007, 43, 42–50. [CrossRef] [PubMed]
10. Nasher, A.T.; Al-Hebshi, N.N.; Al-Moayad, E.E.; Suleiman, A.M. Viral infection and oral habits as risk factors for oral squamous cell carcinoma in Yemen: A case-control study. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2014, 118, 566.e1–572.e1. [PubMed]
11. Muwonge, R.; Ramadas, K.; Sankila, R.; Thara, S.; Thomas, G.; Vinoda, J.; Sankaranarayanan, R. Role of tobacco smoking, chewing and alcohol drinking in the risk of oral cancer in Trivandrum, India: A nested case-control design using incident cancer cases. Oral Oncol. 2008, 44, 446–454. [CrossRef] [PubMed]
12. Znaor, A.; Brennan, P.; Gajalakshmi, V.; Mathew, A.; Shanta, V.; Varghese, C.; Boffetta, P. Independent and combined effects of tobacco smoking, chewing and alcohol drinking on the risk of oral, pharyngeal and esophageal cancers in Indian men. Int J. Cancer 2003, 105, 681–686. [CrossRef] [PubMed]
13. Wei, X.; Deng, X.; Cai, D.; Ji, Z.; Wang, C.; Yu, J.; Li, J.; Chen, S. Decreased tobacco-specific nitrosamines by microbial treatment with Bacillus amyloliquefaciens DA9 during the air-curing process of burley tobacco. J. Agric. Food Chem. 2014, 62, 12701–12706. [CrossRef] [PubMed]
14. Rubinstein, I.; Pedersen, G.W. Bacillus species are present in chewing tobacco sold in the United States and evoke plasma exudation from the oral mucosa. Clin. Diagn. Lab. Immunol. 2002, 9, 1057–1060. [PubMed]
15. Pauly, J.L.; Paszkiewicz, G. Cigarette smoke, bacteria, mold, microbial toxins, and chronic lung inflammation. J. Oncol. 2011, 2011, 819129. [CrossRef] [PubMed]
16. Huang, J.; Yang, J.; Duan, Y.; Gu, W.; Gong, X.; Zhe, W.; Su, C.; Zhang, K.Q. Bacterial diversities on unaged and aging flue-cured tobacco leaves estimated by 16S rRNA sequence analysis. Appl. Microbiol. Biotechnol. 2010, 88, 553–562. [CrossRef] [PubMed]
17. Zhao, M.; Wang, B.; Li, F.; Qiu, L.; Li, F.; Wang, S.; Cui, J. Analysis of bacterial communities on aging flue-cured tobacco leaves by 16S rDNA PCR-DGGE technology. Appl. Microbiol. Biotechnol. 2007, 73, 1435–1440. [CrossRef] [PubMed]
18. Di Giacomo, M.; Paolino, M.; Silvestro, D.; Vigliotta, G.; Imperi, F.; Visca, P.; Alifano, P.; Parente, D. Microbial community structure and dynamics of dark fire-cured tobacco fermentation. Appl. Environ. Microbiol. 2007, 73, 825–837. [PubMed]
19. Su, C.; Gu, W.; Zhe, W.; Zhang, K.Q.; Duan, Y.; Yang, J. Diversity and phylogeny of bacteria on Zimbabwe tobacco leaves estimated by 16S rRNA sequence analysis. Appl. Microbiol. Biotechnol. 2011, 92, 1033–1044. [CrossRef] [PubMed]
20. Law, A.D.; Fisher, C.; Jack, A.; Moe, L.A. Tobacco, Microbes, and Carcinogens: Correlation Between Tobacco Cure Conditions, Tobacco-Specific Nitrosamine Content, and Cured Leaf Microbial Community. Microb. Ecol. 2016, 72, 120–129. [CrossRef] [PubMed]
21. Tyx, R.E.; Stanfill, S.B.; Keong, L.M.; Rivera, A.J.; Satten, G.A.; Watson, C.H. Characterization of Bacterial Communities in Selected Smokeless Tobacco Products Using 16S rDNA Analysis. PLoS ONE 2016, 11, e0146939. [CrossRef] [PubMed]
22. Mizrahi-Man, O.; Davenport, E.R.; Gilad, Y. Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: Evaluation of effective study designs. PLoS ONE 2013, 8, e53608. [CrossRef] [PubMed]
23. Vanwonterghem, I.; Jensen, P.D.; Dennis, P.G.; Hugenholtz, P.; Rabaey, K.; Tyson, G.W. Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters. ISME J. 2014, 8, 2015–2028. [CrossRef] [PubMed]
24. Illumina’s Manual 15044223 Rev. B. Available online: http://support.illumina.com/content/dam/illumina-support/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf (accessed on 17 June 2016).
25. Frank, J.A.; Reich, C.I.; Sharma, S.; Weisbaum, J.S.; Wilson, B.A.; Olsen, G.J. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl. Environ. Microbiol. 2008, 74, 2461–2470. [CrossRef] [PubMed]
26. Lane, D.J.; Pace, B.; Olsen, G.J.; Stahl, D.A.; Sogin, M.L.; Pace, N.R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. USA 1985, 82, 6955–6959. [CrossRef] [PubMed]
27. Zhang, J.; Kobert, K.; Flouri, T.; Stamatakis, A. PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 2014, 30, 614–620. [CrossRef] [PubMed]
28. Schloss, P.D.; Westcott, S.L.; Ryabin, T.; Hall, J.R.; Hartmann, M.; Hollister, E.B.; Lesniewski, R.A.; Oakley, B.B.; Parks, D.H.; Robinson, C.J.; et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75, 7537–7541. [CrossRef] [PubMed]
29. Pruesse, E.; Quast, C.; Knittel, K.; Fuchs, B.M.; Ludwig, W.; Peplies, J.; Glockner, F.O. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35, 7188–7196. [CrossRef] [PubMed]
30. Edgar, R.C.; Haas, B.J.; Clemente, J.C.; Quince, C.; Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27, 2194–2200. [CrossRef] [PubMed]
31. Schloss, P.D.; Gevers, D.; Westcott, S.L. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 2011, 6, e27310. [CrossRef] [PubMed]
32. Al-Hebshi, N.N.; Nasher, A.T.; Idris, A.M.; Chen, T. Robust species taxonomy assignment algorithm for 16S rRNA NGS reads: Application to oral carcinoma samples. J. Oral Microbiol. 2015, 7, 28934. [CrossRef] [PubMed]
33. Human Oral Microbiome Database (HOMD). Available online: http://homd.org/index.php?name=seqDownload&file&type=R (accessed on 29 March 2016).
34. Edgar, R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26, 2460–2461. [CrossRef] [PubMed]
35. Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Pena, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [CrossRef] [PubMed]
36. Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261–5267. [CrossRef] [PubMed]
37. Langille, M.G.; Zaneveld, J.; Caporaso, J.G.; McDonald, D.; Knights, D.; Reyes, J.A.; Clemente, J.C.; Burkepile, D.E.; Vega Thurber, R.L.; Knight, R.; et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013, 31, 814–821. [PubMed]
38. Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsky, L.; Garrett, W.S.; Huttenhower, C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12, R60. [CrossRef] [PubMed]
39. Kozich, J.J.; Westcott, S.L.; Baxter, N.T.; Highlander, S.K.; Schloss, P.D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 2013, 79, 5112–5120. [CrossRef] [PubMed]
40. McMurdie, P.J.; Holmes, S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 2014, 10, e1003531.
41. Stepanov, I.; Jensen, J.; Hatsukami, D.; Hecht, S.S. New and traditional smokeless tobacco: comparison of toxicant and carcinogen levels. Nicotine Tob. Res. 2008, 10, 1773–1782. [PubMed]
42. Hatsukami, D.K.; Ebbert, J.O.; Feuer, R.M.; Stepanov, I.; Hecht, S.S. Changing smokeless tobacco products new tobacco-delivery systems. Am. J. Prev. Med. 2007, 33, S368–S378. [CrossRef] [PubMed]
43. Idris, A.M.; Nair, J.; Ohshima, H.; Friesen, M.; Brouet, I.; Faustman, E.M.; Bartsch, H. Unusually high levels of carcinogenic tobacco-specific nitrosamines in Sudan snuff (toombak). Carcinogenesis 1991, 12, 1115–1118. [PubMed]
44. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans; International Agency for Research on Cancer. Cadmium and cadmium compounds. In A Review of Human Carcinogens: Arsenic, Metals, Fibres and Dusts, Volume 100 C; World Health Organization; distributed by WHO Press: Lyon, France; Geneva, Switzerland, 2012; pp. 121–141.
45. Janbaz, K.H.; Qadir, M.I.; Basser, H.T.; Bokhari, T.H.; Ahmad, B. Risk for oral cancer from smokeless tobacco. Contemp. Oncol. (Pozn.) 2014, 18, 160–164. [CrossRef] [PubMed]
46. Grimsrud, T.K.; Peto, J. Persisting risk of nickel related lung cancer and nasal cancer among Clydach refiners. Occup. Environ. Med. 2006, 63, 365–366. [CrossRef] [PubMed]
47. Su, C.C.; Lin, Y.Y.; Chang, T.K.; Chiang, C.T.; Chung, J.A.; Hsu, Y.Y.; Lian Ie, B. Incidence of oral cancer in relation to nickel and arsenic concentrations in farm soils of patients’ residential areas in Taiwan. BMC Public Health 2010, 10, 67. [CrossRef] [PubMed]
48. Yuan, T.H.; Lian Ie, B.; Tsai, K.Y.; Chang, T.K.; Chiang, C.T.; Su, C.C.; Hwang, Y.H. Possible association between nickel and chromium and oral cancer: A case-control study in central Taiwan. Sci Total Environ. 2011, 409, 1046–1052. [CrossRef] [PubMed]
49. Arain, S.S.; Kazi, T.G.; Afridi, H.I.; Talpur, F.N.; Kazi, A.G.; Brahman, K.D.; Naeemullah Arain, M.S.; Sahito, O.M. Estimation of Nickel in Different Smokeless Tobacco Products and Their Impact on Human Health of Oral Cancer Patients. Nutr. Cancer 2015, 67, 1063–1074. [CrossRef] [PubMed]
50. Andersen, R.A.; Burton, H.R.; Fleming, P.D.; Hamilton-Kemp, T.R. Effect of storage conditions on nitrosated, acylated, and oxidized pyridine alkaloid derivatives in smokeless tobacco products. Cancer Res. 1989, 49, 5895–5900. [PubMed]