Skip to main content
SpringerLink
Log in

Efficacy of indigenous probiotic Lactobacillus strains to reduce cadmium bioaccessibility - An in vitro digestion model

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The toxic heavy metal cadmium (Cd) appears as one of the major global threats to human and animal health. Human being and aquatic life are exposed to Cd by breathing, eating, or drinking when industrial effluents released into environment. The study was aimed to identify cadmium-binding Lactobacillus strain to reduce its bioaccessibility in in vitro digestion model. In this context, forty-eight lactobacilli strains isolated and characterized from fermented dairy products and human origin were screened for their Cd biosorption potential using Flame Atomic Absorption Spectroscopy (FAAS). The present study revealed that Cd biosorption potential of 48 lactobacilli strains ranged from 1.0832 ± 0.012 to 3.562 ± 0.03 mg Cd g−1 of cells from initial 10 mg L−1 cadmium chloride (CdCl2) aqueous solution. Lactobacillus plantarum strain HD 48 demonstrated highest biosorption of 3.562 ± 0.03 mg Cd g−1 of cells. Lactobacilli-Cd complex stability indicated its strong stability as even after three washes with Milli-Q water metal desorption was nonsignificant (p < 0.05) and further studies to delineate the influence of Cd (100 mg L−1 CdCl2) on their growth. Moreover, these strains were able to reduce Cd bioaccessibility in the in vitro digestion model in the range of 24.71 to 41.62 %. Transmission electron microscopy (TEM) investigations on Cd bioadsorption also revealed its surface associated bioadsorption phenomenon. These findings depicted that probiotic strain L. plantarum HD 48 was found to be endowed with remarkable Cd biosorption ability as well as reduction in its bioaccessibility. These results suggest that probiotic strain L. plantarum HD 48 has immense potential to sequester Cd from aqueous solution which could be further explored as a potent source to diminish body Cd burden.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2a, b
Fig. 3
Fig. 4
Fig. 5
Fig. 6 a–c

Similar content being viewed by others

References

  • Amiard JC, Amiard-Triquet C, Charbonnier L, Mesnil A, Rainbow PS, Wang WX (2008) Bioaccessibility of essential and non-essential metals in commercial shellfish from Western Europe and Asia. Food Chem Toxicol 46(6):2010–2022. doi:10.1016/j.fct.2008.01.041

    Article  CAS  Google Scholar 

  • Arauz ILC, Afton S, Wrobel K, Caruso JA, Corona J, Wrobel K (2008) Study on the protective role of selenium against cadmium toxicity in lactic acid bacteria: an advanced application of ICP-MS. J Hazard Mater 153(3):1157–1164. doi:10.1016/j.jhazmat.2007.09.075

    Article  CAS  Google Scholar 

  • Baldwin DR, Marshall WJ (1999) Heavy metal poisoning, and its laboratory investigation. Ann Clin Biochem 36:267–300. doi:10.1177/000456329903600301

    Article  CAS  Google Scholar 

  • Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei MQ (2012) Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. J Appl Microbiol 112(6):1193–1206. doi:10.1111/j.1365-2672.2012.05284.x

    Article  CAS  Google Scholar 

  • Brahma B, Patra MC, Karri S, Chopra M, Mishra P, De BC, Kumar S, Mahanty S, Thakur K, Poluri KM, Datta TK (2015) Diversity, antimicrobial action and structure-activity relationship of buffalo Cathelicidins. PLoS One 10(12):e0144741. doi:10.1371/journal.pone.0144741

    Article  Google Scholar 

  • Buckler HM, Smith WDF, Rees WDW (1986) Self-poisoning with oral cadmium chloride. Br Med J 292:1559–1560. doi:10.1136/bmj.292.6535.1559

    Article  CAS  Google Scholar 

  • Dorta DJ, Leite S, DeMarco KC, Prado IM, Rodrigues T, Mingatto FE, Uyemura SA, Santos AC, Curti C (2003) A proposed sequence of events for cadmium-induced mitochondrial impairment. J Inorg Biochem 97(3):251–257. doi:10.1016/S0162-0134(03)00314-3

    Article  CAS  Google Scholar 

  • Doyle JJ, Marshall RT, Pfander WH (1975) Effects of cadmium on the growth and uptake of microorganisms. Appl Microbiol 29(4):562–564

    CAS  Google Scholar 

  • El-Helow ER, Sabry SA, Amer RM (2000) Cadmium biosorption by a cadmium resistant strain of Bacillus thuringiensis: regulation and optimization of cell surface affinity for metal cations. Biometals 13(4):273–280. doi:10.1023/A:1009291931258

    Article  CAS  Google Scholar 

  • Faroon O, Ashizawa A, Wright S, Tucker P, Jenkins K, Ingerman L, Rudisill C (2012) Toxicological profile for cadmium. Agency for Toxic Substances and Disease Registry (ATSDR), Atlanta, GA.

  • Fazeli M, Hassanzadeh P, Alaei S (2011) Cadmium chloride exhibits a profound toxic effect on bacterial microflora of the mice gastrointestinal tract. Hum Exp Toxicol 30(2):152–159. doi:10.1177/0960327110369821

    Article  CAS  Google Scholar 

  • Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. Journal of occupational medicine and toxicology 1(1):1. doi:10.1186/1745-6673-1-22

    Article  Google Scholar 

  • Gulnaz O, Saygideger S, Kusvuran E (2005) Study of Cu (II) biosorption by dried activated sludge: effect of physico-chemical environment and kinetics study. J Hazard Mater 120(1):193–200. doi:10.1016/j.jhazmat.2005.01.003

    Article  CAS  Google Scholar 

  • Halttunen T, Salminen S, Tahvonen R (2007) Rapid removal of lead and cadmium from water by specific lactic acid bacteria. Int J Food Microbiol 114:30–35. doi:10.1016/j.ijfoodmicro.2006.10.040

    Article  CAS  Google Scholar 

  • Halttunen T, Salminen S, Meriluoto RJ, Kalle LT (2008) Reversible surface binding of cadmium and lead by lactic acid and bifidobacteria. Int J Food Microbiol 125:170–175. doi:10.1016/j.ijfoodmicro.2008.03.041

    Article  Google Scholar 

  • Ibrahim F, Halttunen T, Tahvonen R, Salminen S (2006) Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Can J Microbiol 52:877–885. doi:10.1139/W06-043

    Article  CAS  Google Scholar 

  • Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60–72. doi:10.2478/intox-2014-0009

    Article  Google Scholar 

  • Jarup L, Alfven T (2004) Low level cadmium exposure, renal and bone effects—the OSCAR study. Biometals 17(5):505–509. doi:10.1023/B:BIOM.0000045729.68774.a1

    Article  Google Scholar 

  • Kabak B, Ozbey F (2012) Aflatoxin M1 in UHT milk consumed in Turkey and first assessment of its bioaccessibility using an in vitro digestion model. Food Control 28(2):338–344. doi:10.1016/j.foodcont.2012.05.029

    Article  CAS  Google Scholar 

  • Kaewsarn P, Yu Q (2001) Cadmium (II) removal from aqueous solutions by pre-treated biomass of marine alga Padina sp. Environ Pollut 112(2):209–213. doi:10.1016/S0269-7491(00)00114-7

    Article  CAS  Google Scholar 

  • Kinoshita H, Sohma Y, Ohtake F, Ishida M, Kawai Y, Kitazawa H, Saito T, Kimura K (2013) Biosorption of heavy metals by lactic acid bacteria and identification of mercury binding protein. Res Microbiol 164:701–709. doi:10.1016/j.resmic.2013.04.004

    Article  CAS  Google Scholar 

  • Kobayashi E, Suwazono Y (2009) Estimation of benchmark rice cadmium doses as threshold values for abnormal urinary findings with adjustment for consumption of Jinzu River water. Bull Environ Contam Toxicol 83:102–107. doi:10.1007/s00128-009-9766-9

    Article  CAS  Google Scholar 

  • Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238:209–214. doi:10.1016/j.taap.2009.01.029

    Article  CAS  Google Scholar 

  • Meriluoto J, Codd GA (2005) Cyanobacterial monitoring and cyanotoxin analysis. Acta Academiae Aboensis 65(1):1–145. doi:10.3390/toxins7062198

    Google Scholar 

  • Monachese M, Burton JP, Reid G (2012) Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics? Appl Environ Microbiol 78(18):6397–6404. doi:10.1128/AEM.01665-12

    Article  CAS  Google Scholar 

  • Oomen AG, Rompelberg CJ, Bruil MA, Dobbe CJ, Pereboom DP, Sips AJ (2003) Development of an in vitro digestion model for estimating the bioaccessibility of soil contaminants. Arch Environ Contam Toxicol 44(3):0281–0287. doi:10.1007/s00244-002-1278-0

    Article  CAS  Google Scholar 

  • Satarug S, Moore MR (2004) Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ Health Perspect 112(10):1099–1103. doi:10.1289/ehp.6751

    Article  CAS  Google Scholar 

  • Satarug S, Garrett SH, Sens MA, Sens DA (2011) Cadmium, environmental exposure, and health outcomes. Ciencia & saude coletiva 16(5):2587–2602. doi:10.1289/ehp.0901234

    Article  Google Scholar 

  • Serrano-Nino JC, Cavazos-Garduno A, Hernandez-Mendoza A, Applegate B, Ferruzzi MG, San Martin-González MF, García HS (2013) Assessment of probiotic strains ability to reduce the bioaccessibility of aflatoxin M1 in artificially contaminated milk using an in vitro digestive model. Food Control 31(1):202–207. doi:10.1016/j.foodcont.2012.09.023

    Article  CAS  Google Scholar 

  • Sharma S, Prasad FM (2010) Accumulation of lead and cadmium in soil and vegetable crops along major highways in Agra (India). Journal of. Chemistry 7(4):1174–1183. doi:10.1155/2010/678589

    CAS  Google Scholar 

  • Sharma RK, Agrawal M, Marshall FM (2009) Heavy metals in vegetables collected from production and market sites of a tropical urban area of India. Food Chem Toxicol 47(3):583–591. doi:10.1016/j.fct.2008.12.016

    Article  CAS  Google Scholar 

  • Singh A, Sharma RK, Agrawal M, Marshall FM (2010) Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food Chem Toxicol 48(2):611–619. doi:10.1016/j.fct.2009.11.041

    Article  CAS  Google Scholar 

  • Staessen JA, Thijs L, Fagard R, O'Brien ET, Clement D, de Leeuw PW, Mancia G, Nachev C, Palatini P, Parati G, Tuomilehto J (1999) Predicting cardiovascular risk using conventional vs ambulatory blood pressure in older patients with systolic hypertension. JAMA 282(6):539–546. doi:10.1001/jama.282.6.539

    Article  CAS  Google Scholar 

  • Sun L, Liu G, Yang M, Zhuang Y (2012) Bioaccessibility of cadmium in fresh and cooked Agaricus blazei Murill assessed by in vitro biomimetic digestion system. Food Chem Toxicol 50(5):1729–1733. doi:10.1016/j.fct.2012.02.044

    Article  CAS  Google Scholar 

  • Tian F, Xiao Y, Li X, Zhai Q, Wang G, Zhang Q, Zhang H, Chen W (2015) Protective effects of Lactobacillus plantarum CCFM8246 against copper toxicity in mice. PLoS One 10(11):e0143318. doi:10.1371/journal.pone.0143318

    Article  Google Scholar 

  • Topcu A, Bulat T (2010) Removal of cadmium and lead from aqueous solution by Enterococcus faecium strains. J Food Sci 75:T13–T17. doi:10.1111/j.1750-3841.2009.01429.x

    Article  CAS  Google Scholar 

  • Uttara B, Singh AV, Zamboni P, Mahajan R (2009) Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 7(1):65–74. doi:10.2174/157015909787602823

    Article  CAS  Google Scholar 

  • Veglio F, Beolchini F (1997) Removal of metals by biosorption: a review. Hydrometallurgy 44(3):301–316. doi:10.1016/S0304-386X (96)00059-x

    Article  CAS  Google Scholar 

  • Veglio F, Beolchini F, Gasbarro A (1997) Biosorption of toxic metals: an equilibrium study using free cells of Arthrobacter sp. Process Biochem 32(2):99–105. doi:10.1016/S0032-9592(96)00047-7

    Article  CAS  Google Scholar 

  • Versantvoort CH, Oomen AG, Van de Kamp E, Rompelberg CJ, Sips AJ (2005) Applicability of an in vitro digestion model in assessing the bioaccessibility of mycotoxins from food. Food Chem Toxicol 43(1):31–40

    Article  CAS  Google Scholar 

  • Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8(1):121–135. doi:10.1016/S1093-0191(02)00135-1

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Ism Ecology. doi:10.5402/2011/402647

    Google Scholar 

  • Yadav A, Yadav PK, Shukla DN (2013) Investigation of heavy metal status in soil and vegetables grown in urban area of Allahabad, Uttar Pradesh, India. International Journal of Scientific and Research Publications 3(9):1–7.

  • Yang LS, Zhang XW, Li YH, Li HR, Wang Y, Wang WY (2011) Bioaccessibility and risk assessment of cadmium from uncooked rice using an in vitro digestion model. Biol Trace Elem Res 145(1):81–86. doi:10.1007/s12011-011-9159-x

    Article  Google Scholar 

  • Zhai Q, Wang G, Zhao J, Liu X, Tian F, Zhang H, Chen W (2013) Protective effects of Lactobacillus plantarum CCFM8610 against acute cadmium toxicity in mice. Appl Environ Microbiol 79(5):1508–1515. doi:10.1128/AEM.03417-12

    Article  CAS  Google Scholar 

  • Zhai Q, Wang G, Zhao J, Liu X, Narbad A, Chen YQ, Zhang H, Tian F, Chen W (2014) Protective effects of Lactobacillus plantarum CCFM8610 against chronic cadmium toxicity in mice: Intestinal sequestration is not the only route of protection. Applied and environmental microbiology. AEM-00762. doi.org/10.1128/AEM.00762-14

  • Zhai Q, Yin R, Yu L, Wang G, Tian F, Yu R, Zhao J, Liu X, Chen YQ, Zhang H, Chen W (2015) Screening of lactic acid bacteria with potential protective effects against cadmium toxicity. Food Control 54:23–30. doi:10.1039/C4RA12865F

    Article  CAS  Google Scholar 

  • Zhang WL, Du Y, Zhai MM, Shang Q (2014) Cadmium exposure and its health effects: a 19-year follow-up study of a polluted area in China. Sci Total Environ 470:224–228. doi:10.1016/j.scitotenv.2013.09.070

    Article  Google Scholar 

  • Zhuang P, McBride MB, Xia H, Li N, Li Z (2009) Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. Sci Total Environ 407(5):1551–1561. doi:10.1016/j.scitotenv.2008.10.061

    Article  CAS  Google Scholar 

  • Zoghi A, Khosravi-Darani K, Sohrabvandi S (2014) Surface binding of toxins and heavy metals by probiotics. Mini reviews in medicinal chemistry 14(1):84–98. doi:10.2174/1389557513666131211105554

    Article  CAS  Google Scholar 

  • Zoumpopoulou G, Foligne B, Christodoulou K, Grangette C, Pot B, Tsakalidou E (2008) Lactobacillus fermentum ACA-DC 179 displays probiotic potential in vitro and protects against trinitrobenzene sulfonic acid (TNBS)-induced colitis and salmonella infection in murine models. Int J Food Microbiol 121(1):18–26. doi:10.1016/j.ijfoodmicro.2007.10.013

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The authors acknowledge the Director, ICAR-National Dairy Research Institute (NDRI) Karnal-132001, (Haryana), India. The first author also acknowledges University Grant Commission (UGC) for the financial support in terms of all India fellowship (RGNF-SRF). We greatly acknowledge the help rendered by Mr. Rajkumar for providing AAS facility at ICAR-Central Soil Salinity Research Institute, Karnal-132001, (Haryana) INDIA and Devashish Dewedi for help in designing this project.

Author information

Authors and Affiliations

  1. Synbiotic Functional Foods Laboratory, Dairy Microbiology Division, ICAR-National Dairy Research Institute, Karnal, Haryana, 132001, India

    Narendra Kumar, Rohit Panwar & Chand Ram

  2. RK University, Bhavnagar Highway, Kasturbadham Rajkot, Gujarat, 360020, India

    Vijay Kumar

Authors
  1. Narendra Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vijay Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rohit Panwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chand Ram
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chand Ram.

Ethics declarations

Author contributions

Narendra Kumar: Conceived the work, design the whole experiment and statistical analysis of the experimental data. The manuscript was seriously written by Narendra Kumar. Rohit Panwar was involved in the preparation of media and acid washing of glass wares.

Chand ram and Vijay Kumar: Provided technical suggestions and critically reviewed the manuscript to improve the overall quality of the article. The grammatical and language improvement was also done.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Editorial responsibility: Philippe Garrigues

Electronic supplementary material

ESM 1

(DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, N., Kumar, V., Panwar, R. et al. Efficacy of indigenous probiotic Lactobacillus strains to reduce cadmium bioaccessibility - An in vitro digestion model. Environ Sci Pollut Res 24, 1241–1250 (2017). https://doi.org/10.1007/s11356-016-7779-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7779-6

Keywords

Search

Navigation