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Influence of Environmental Factors on Salivary Microbiota and Their Metabolic Pathway: Next-Generation Sequencing Approach

  • Human Microbiome
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Abstract

The current study aimed to investigate the effect of periodontitis and long-term heavy metal (HM) exposure on the salivary microbiome. The patients were divided into four groups as Wu Wei control (WWC) group involved healthy individuals, Wu Wei periodontitis (WWP) patients having periodontitis, Jing Chang with metal pollution periodontally healthy individuals (JCP), and Kuang periodontitis (KP). The most abundant bacteria identified at the phylum level in the WWC group were Bacteroides, Firmicutes, and Fusobacteria. Firmicutes were observed in a significantly higher proportion in the KP group than in the WWC, WWP, and JCP. At the genus level, the WWC has major dominating bacterial genera (such as Leptotrichia, Neisseria, and Fusobacterium) which were similar to WWP and KP group. The significant difference (p < 0.05) was found in alpha diversity while in beta diversity, the significant (p = 0.005) results were found among the four groups. The correlation of oral microbiota revealed that HMs present in the soil (Cr, Ni, and Cu) are associated with the growth of Capnocytophaga, Selenomonas, Aggregatibacter, and Campylobacter. The bacterial functions in the KP group were higher in translation and nucleotide metabolism than in the WWP group. This demonstrated that long-term exposure to HMs can influence the salivary microbiota which can alter the functioning, and diversity of bacteria.

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Data Availability

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi. nlm.nih.gov/sra/PRJNA721290.

Code Availability

Not applicable.

References

  1. Zhang J, Li X, Guo L, Deng Z, Wang D, Liu L (2021) Assessment of heavy metal pollution and water quality characteristics of the reservoir control reaches in the middle Han River. China. Sci. Total Environ. 799:149472

    Article  CAS  Google Scholar 

  2. Azimi A, Azari A, Rezakazemi M, Ansarpour M (2017) Removal of heavy metals from industrial wastewaters: a review. Chembioeng Rev 4:37–59

    Article  Google Scholar 

  3. Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip. Toxicol. 60–72

  4. Jian MF, Ling-Yu LI, Peng-Fei XU, Chen PQ, Xiong JQ, Zhou XL (2014) Spatiotemporal variation characteristics of heavy metals pollution in the water, soil and sediments environment of the Lean River-Poyang Lake Wetland. Environ Sci 35:1759

    Google Scholar 

  5. Ciurli, Stefano, Zambelli, Barbara, Uversky, Vladimir, and N. (2016) Nickel impact on human health: an intrinsic disorder perspective. Biochim. Biophys. Acta. Proteins Proteom. 1714–1731

  6. Kang Y, Sun B, Chen Y, Lou Y, Zheng M, Li Z (2021) Dental plaque microbial resistomes of periodontal health and disease and their changes after scaling and root planing therapy. mSphere 6:e0016221–e0016221

    Article  Google Scholar 

  7. Kinane DF, Stathopoulou PG, Papapanou PN (2017) Authors’ reply: Predictive diagnostic tests in periodontal diseases. Nat Rev Dis Primers 3:17070

    Article  Google Scholar 

  8. Kim Y, Lee BKJIAoO, Health E, (2013) Association between blood lead and mercury levels and periodontitis in the Korean general population: analysis of the 2008–2009 Korean National Health and Nutrition Examination Survey data. Int Arch Occup Environ Health 86:607–613

    Article  CAS  Google Scholar 

  9. Duarte PM, Nogueira CFP, Silva SM, Pannuti CM, Schey KC, Miranda TS (2021) Impact of smoking cessation on periodontal tissues. Int. Dental J. 1–6.

  10. Zhao H, Wang Y, Shao Y, Liu J, Wang S, Xing MJC (2018) Oxidative stress-induced skeletal muscle injury involves in NF-κB/p53-activated immunosuppression and apoptosis response in copper (II) or/and arsenite-exposed chicken. Chemosphere 210:76

    Article  CAS  Google Scholar 

  11. Bai Y, Yang A, Pu H, Min D, Ning C, Jiao D, Li J, Li H, Hu X, Ren X (2016) Cohort profile: the China metal-exposed workers cohort study (Jinchang cohort). Int. J. Epidemiol.:dyw223

  12. Ji Y, Liang X, Lu H (2020) Analysis of by high-throughput sequencing: Helicobacter pylori infection and salivary microbiome. BMC Oral Health 20:84

    Article  Google Scholar 

  13. Chen H, Jiang W (2014) Application of high-throughput sequencing in understanding human oral microbiome related with health and disease. Front Microbiol 5:508

    Article  Google Scholar 

  14. Cao Y, Min Q, Tian Z, Yan Y, Xu B, Lao W, Ma X, Li W (2018) Comparative analyses of subgingival microbiome in chronic periodontitis patients with and without IgA nephropathy by high throughput 16S rRNA sequencing. Cell Physiol Biochem 47:774–783

    Article  CAS  Google Scholar 

  15. Aljehani YA (2014) Risk factors of periodontal disease: review of the literature. Int J Dent 2014:182513

    Article  Google Scholar 

  16. Schmidt BL, Justin K, Aditi B, Bing H, Corby PM, Queiroz ELS, Kira N, Ross KA, Delacure MD, Ratna V (2014) Changes in abundance of oral microbiota associated with oral cancer. Plos One 9:e98741

    Article  Google Scholar 

  17. Wang J, Qi J, Zhao H, He S, Zhang Y, Wei S, Zhao F (2013) Metagenomic sequencing reveals microbiota and its functional potential associated with periodontal disease. Sci Rep 3:1843

    Article  Google Scholar 

  18. Perez-Chaparro PJ, Goncalves C, Figueiredo LC, Faveri M, Lobao E, Tamashiro N, Duarte P, Feres M (2014) Newly identified pathogens associated with periodontitis: a systematic review. J Dent Res 93:846

    Article  CAS  Google Scholar 

  19. Haffajee AD, Bogren A, Hasturk H, Feres M, Lopez NJ, Socransky SS (2004) Subgingival microbiota of chronic periodontitis subjects from different geographic locations. J. Clin. Periodontol.

  20. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ (2003) New bacterial species associated with chronic periodontitis. J Dent Res 82:338

    Article  CAS  Google Scholar 

  21. Caufield PW, Schon CN, Saraithong P, Li Y, Argimon S (2015) Oral lactobacilli and dental caries: a model for niche adaptation in humans. J. Dent. Res.: 110S.

  22. Adrián T, Juan A, Jaume L, Pericàs JM, Carles F, Manel A, Cristina GdlM, Marta HM, Bàrbara V, Elena S (2017) Epidemiology, clinical features and outcome of infective endocarditis due to Abiotrophia spp. and Granulicatella spp. Report of 76 cases (2000–2015). Clin. Infec.t Dis.1:104–111

  23. Qi Y, Zang S-q, Wei J, Yu H-c, Yang Z, Wu H-m, Kang Y, Tao H, Yang M-f, Jin L, Zen K, Wang F-y (2021) High-throughput sequencing provides insights into oral microbiota dysbiosis in association with inflammatory bowel disease. Genomics 113:664–676

    Article  CAS  Google Scholar 

  24. Ge X, Rodriguez R, Trinh M, Gunsolley J, Xu P (2013) Oral microbiome of deep and shallow dental pockets in chronic periodontitis. Plos One 8:e65520

    Article  CAS  Google Scholar 

  25. De Filippis F, Vannini L, La Storia A, Laghi L, Piombino P, Stellato G, Serrazanetti DI, Gozzi G, Turroni S, Ferrocino I, Lazzi C, Di Cagno R, Gobbetti M, Ercolini D (2014) The same microbiota and a potentially discriminant metabolome in the saliva of omnivore, ovo-lacto-vegetarian and Vegan individuals. PLoS One 9:e112373

    Article  Google Scholar 

  26. Krishnan K, Chen T, Paster B (2016) A practical guide to the oral microbiome and its relation to health and disease. Oral Dis.

  27. Pedro, Bullon, Luis, Pavillard, Rafael, de, la, Torre-Torres (2018) Inflammasome and oral diseases. Exp. Suppl. 153–176.

  28. Costalonga M, Herzberg MC (2014) The oral microbiome and the immunobiology of periodontal disease and caries. Immunol Lett 162:22–38

    Article  CAS  Google Scholar 

  29. Abdelhamid AJIJH (2016) Effect of exposure to portland cement dust on the periodontal status and on the outcome of non-surgical periodontal therapy. Int J Health Sci 10:339–352

    Google Scholar 

  30. El-Said KF, El-Ghamry AM, Mahdy NH, El-Bestawy NA (2008) Chronic occupational exposure to lead and its impact on oral health. J Egypt Public Health Assoc 83:451–466

    Google Scholar 

  31. Mahtout H, Chandad F, Rojo JM, Grenier D (2009) Porphyromonas gingivalis mediates the shedding and proteolysis of complement regulatory protein CD46 expressed by oral epithelial cells. Oral Microbiol Immunol 24:396–400

    Article  CAS  Google Scholar 

  32. Saraiva MCP, Taichman RS, Braun T, Nriagu JO, Burt B (2010) Lead exposure and periodontitis in US adults. J Periodontal Res 42:45–52

    Article  Google Scholar 

  33. Ayansina A, Olubukola B (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health. 19:14

    Google Scholar 

  34. Mystkowska J (2016) Biocorrosion of dental alloys due to Desulfotomaculum nigrificans bacteria. Acta Bioeng Biomech 18:87–96

    Google Scholar 

  35. Lu K, Abo RP, Schlieper KA, Graffam ME, Levine S, Wishnok JS, Swenberg JA, Tannenbaum SR, Fox JG (2014) Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ Health Perspect 122:284

    Article  CAS  Google Scholar 

  36. Li X, Brejnrod AD, Ernst M, Rykaer M, Srensen SJJEI (2019) Heavy metal exposure causes changes in the metabolic health-associated gut microbiome and metabolites. Environ Int 126:454–467

    Article  CAS  Google Scholar 

  37. Hsieh YY, Tung SY, Pan HY, Yen CW, Li C (2018) Increased abundance of Clostridium and Fusobacterium in gastric microbiota of patients with gastric cancer in Taiwan. Sci. Rep. 8.

  38. Wang L, Yin X, Gao S, Jiang T, Ma CJC (2020) In vitro oral bioaccessibility investigation and human health risk assessment of heavy metals in wheat grains grown near the mines in North China. Chemosphere. 252:126522

    Article  CAS  Google Scholar 

  39. Filoche S, Wong L, Sissons CH (2010) Oral biofilms: emerging concepts in microbial ecology. J dent Res 89:8–18

    Article  CAS  Google Scholar 

  40. Wells JC, Sawaya AL, Wibaek R, Mwangome M, Demaio A (2019) The double burden of malnutrition: aetiological pathways and consequences for health. Lancet (London, England) 395.

  41. Zhang Y, Huo X, Lu X, Zeng Z, Xu X (2020) Exposure to multiple heavy metals associate with aberrant immune homeostasis and inflammatory activation in preschool children. Chemosphere 257:127257

    Article  CAS  Google Scholar 

  42. Wu Z, Hao Z, Sun Y, Guo L, Chen B (2016) Comparison on the structure and function of the rhizosphere microbial community between healthy and root-rot Panax notoginseng. Appl Soil Ecol 107:99–107

    Article  Google Scholar 

  43. Mihaila D, Donegan J, Barns S, LaRocca D, Du Q, Zheng D, Vidal M, Neville C, Uhlig R, Middleton FA (2019) The oral microbiome of early stage Parkinson’s disease and its relationship with functional measures of motor and non-motor function. PLoS One 14:e0218252

    Article  CAS  Google Scholar 

  44. Corrêa JD, Fernandes GR, Calderaro DC, Mendona SMS, Graves DT (2019) Oral microbial dysbiosis linked to worsened periodontal condition in rheumatoid arthritis patients. Sci. Rep. 9.

  45. Abdelhamid A (2016) Effect of exposure to Portland cement dust on the periodontal status and on the outcome of non-surgical periodontal therapy. Int J Health Sci (Qassim) 10:339–352

    Google Scholar 

  46. Davis E, Bakulski KM, Goodrich JM, Peterson KE, Marazita ML, Foxman B (2020) Low levels of salivary metals, oral microbiome composition and dental decay. Sci Rep 10:14640

    Article  CAS  Google Scholar 

  47. Li X, Meng D, Li J, Yin H, Liu H, Liu X, Cheng C, Xiao Y, Liu Z, Yan M (2017) Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environ Pollut 231:908–917

    Article  CAS  Google Scholar 

Download references

Funding

This study was financially supported by the National Natural Science Foundation of China (31500412), National Natural Science Foundation of Gansu Province, China (20JR5RA327, 21JR1RA152), and Lanzhou science and technology plan project (2018–4-66).

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Author notes

  1. Wei Zhang and Tao Qi contributed equally to this work and can be regarded as the co-first authors.

Authors and Affiliations

  1. Healthy Dental Clinic, Healthy Examination & Management Center of Lanzhou University Second Hospital, Lanzhou, China

    Wei Zhang

  2. Department of Stomatology, First Hospital of Lanzhou University, Lanzhou, China

    Tao Qi

  3. Department of Neurology, First Hospital of Lanzhou University, Lanzhou, China

    Lihe Yao

  4. School of Stomatology, Lanzhou University, Lanzhou, China

    Wei Wang, Fanrong Yu & Yuqin Yan

  5. Department of Occupational and Environmental Health, School of Public Health, Lanzhou University, Lanzhou, 730000, Gansu Province, People’s Republic of China

    El-Sayed Salama

  6. Healthy Examination & Management Center, First Hospital of Lanzhou University, Lanzhou, China

    Shaochen Su

  7. Department of Cardiology, First Hospital of Lanzhou University, LanzhouGansu, 730000, China

    Ming Bai

Authors
  1. Wei Zhang
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  2. Tao Qi
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  4. Wei Wang
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Contributions

Wei Zhang: methodology, visualization, investigation, data curation, formal analysis, writing, original draft. Tao Qi: investigation, data curation, formal analysis, writing — review and editing. Lihe Yao: visualization, formal analysis. Wei Wang: visualization, formal analysis. Fanrong Yu: visualization, formal analysis. Yuqin Yan: investigation, data curation, formal analysis. El-Sayed Salama: data curation, validation, visualization, formal analysis, writing — review and editing. Shaochen Su: conceptualization, supervision, resources, data curation, validation, writing — review and editing, funding acquisition, project administration. Ming Bai: conceptualization, supervision, resources, data curation, validation, writing — review and editing.

Corresponding authors

Correspondence to Shaochen Su or Ming Bai.

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The authors declare no competing interests.

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Zhang, W., Qi, T., Yao, L. et al. Influence of Environmental Factors on Salivary Microbiota and Their Metabolic Pathway: Next-Generation Sequencing Approach. Microb Ecol 85, 317–329 (2023). https://doi.org/10.1007/s00248-021-01951-0

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  • DOI: https://doi.org/10.1007/s00248-021-01951-0

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