Abstract
Arsenic (As) contamination of water and food is a global problem posing a severe threat to environmental and human health; therefore, fish as an aquatic animal is immensely affected by the hazardous impacts of As. The present study aimed to explore the As-resistant probiotic bacteria and characterize their potential for applying as an As bioremediation tool in fish. As-resistant lactic acid bacteria (LAB) were isolated from sludge samples of an old stabilization pond/lagoon of wastewater treatment plant using spared plate techniques. The potential probiotic was selected by assessing the sequential probiotic characterization, As resistance and removal properties. The selected probiotic was identified by PCR-based molecular method using 16S rDNA. A total of 51 As-resistant LAB were isolated from sludge samples. Potential six As-resistant LAB strains (As4, 11, 20, 21, 41 and 48) were selected from 51 isolates through sequential probiotic characterizations using mimic fish gastrointestinal conditions. The selected probiotics displayed relatively elevated As (> 1000 mg L−1), cadmium (20–100 mg L−1) and lead (> 2000 mg L−1)–resistant patterns and excellent As-removal efficiencies (0.0012–0.0044 mg As mg cell−1 h−1) from water along with favourable various associative probiotic properties. The 16S rDNA sequence-based molecular identification and phylogenetic analysis revealed that the strains As4, 11, 20, 21, 41 and 48 belong to Limosilactobacillus fermentum (Lactobacillus fermentum according to old taxonomy). The As removal and survival in mimic gastrointestinal conditions of fish indicated that new Limosilactobacillus fermentum strains could be employed as the novel and potential probiotic tools for possible bioremediation of As and other pollutants in the fish to prevent the bioaccumulation and toxicity impacts of As in fish for cleaner and safe fish food production.
Similar content being viewed by others
Data Availability
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request. All data generated or analysed during this study are included in this published article
References
Bagchi S (2007) Arsenic threat reaching global dimensions. Can Med Assoc J 177:1344–1345. https://doi.org/10.1503/cmaj.071456
Howard G (2003) Arsenic, drinking-water and health risk substitution in arsenic mitigation: a discussion paper. World Health Organization, Geneva. https://cdn.who.int/media/docs/default-source/wash-documents/water-safety-and-quality/wsh03.06fulltext.pdf?sfvrsn=3e67a751_3
WHO (World Health Organization) (2011) Arsenic in drinking-water (background document for development of WHO Guidelines for Drinking-water Quality). WHO Press, Geneva, Switzerland. https://www.who.int/water_sanitation_health/dwq/chemicals/arsenic.pdf
Murphy BL, Toole AP, Bergstrom PD (1989) Health risk assessment for arsenic contaminated soil. Environ Geochem Heal 11:163–169. https://doi.org/10.1007/BF01758667
Hemond HM, Gabriele Solo HF (2004) Children’s exposure to arsenic from CCA-treated wooden decks and playground structures. Risk Anal 24:51–64. https://doi.org/10.1111/j.0272-4332.2004.00411.x
Bhakta JN, Son LT, Munekage Y (2009) Distribution and potential impact of metal pollutants in the coastal environment: a case study with special reference to coastal aquaculture in red river delta of Viet Nam. Elect J of Biol 5:22–27
Ahmad SA, Khan MH (2015) Ground water arsenic contamination and its health effects in Bangladesh. In: Flora S.J.S. (Ed.), Handbook of Arsenic Toxicology. Academic Press Publishers, USA, pp 51–72. https://doi.org/10.1016/B978-0-12-418688-0.00002-2
Bhakta JN, Rana S, Jana J, Bag SK, Lahiri S, Jana BB, Panning F, Fechter F (2016) Current status of arsenic contamination in drinking water and treatment practice in some rural areas of West Bengal, India. J Wat Chem Tech 38:366–373. https://doi.org/10.3103/S1063455X16060114
Ahmad SA, Khan MH, Haque M (2018) Arsenic contamination in groundwater in Bangladesh: implications and challenges for healthcare policy. Risk Manag Health Pol 112:251–261. https://doi.org/10.2147/RMHP.S153188
Gupta SK, Chen KY (1978) Arsenic removal by adsorption. J Water Pollut Control Fed 50:493–506
Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235. https://doi.org/10.1016/S0039-9140(02)00268-0
Robertson FN (1989) Arsenic in ground-water under oxidizing conditions, south-west United States. Environ Geochem Heal 11:171–185. https://doi.org/10.1007/BF01758668
NAS (National Academy of Sciences) (1977) Arsenic-medical and biological effects of environmental pollutants. U.S. Government Printing Office, Washington, DC, USA. https://doi.org/10.17226/9003
USEPA (U.S. Environmental Protection Agency) (1988) Special report on ingested inorganic arsenic: skin cancer; nutritional essentiality. EPA 625/3–87/013. U.S. Environmental Protection Agency, Risk Assessment Forum, Washington, DC, USA
NRC (National Research Council) (1999) Arsenic in drinking water. National Academy Press, Washington, DC, USA. https://doi.org/10.17226/6444
Bhakta JN, Munekage Y (2009) Effects of some metal oxides in Arsenic removal capacity of soil from aquatic environment, In: Khan R, Harooqi RH, Basheer F (eds) Proceedings of International Conference on Emerging Technologies in Environmental Science and Engineering, Aligarh Muslim University, India, pp 575–582
Bhakta JN, Munekage Y, Ohnishi K, Jana BB (2012) Isolation and identification of cadmium and lead resistant lactic acid bacteria for applying as metal removing probiotic. Int J Env Sci Tech 9:433–440. https://doi.org/10.1007/s13762-012-0049-3
Bunting SW, Pretty J, Edwards P (2010) Wastewater-fed aquaculture in the East Kolkata Wetlands, India: anachronism or archetype for resilient ecocultures? Rev Aquac 2(3):138–153. https://doi.org/10.1111/J.1753-5131.2010.01
Edwards P (2005) Demise of periurban wastewater-fed aquaculture? Urban Agric Mag 14:27–29
Edwards P (2005) Development status of, and prospects for, wastewater-fed aquaculture in urban environments. In: Costa-Pierce B, Desbonnet A, Edwards P, Baker D (eds) Urban aquaculture. CABI Publishing, Wallingford, pp 45–59
Jana BB (1998) Sweage-fed aquaculture: the Calcutta model1. Ecol Eng 11:73–85. https://doi.org/10.1016/S0925-8574(98)00024-X
Phuong NTD, Tuan PA (2005) Current status of periurban aquatic production in Hanoi. Urban Agric Mag 14:10–12
Long A, Wang W-X (2005) Assimilation and bioconcentration of Ag and Cd by the marine black bream after waterborne and dietary metal exposure. Environ Toxicol Chem 24:709–716. https://doi.org/10.1897/03-664.1
Marcussen H, Holm PE, Ha LT, Dalsgaard A (2007) Food safety aspects of toxic element accumulation in fish from wastewater fed ponds in Hanoi. Vietnam Trop Med Int Health 12:34–39. https://doi.org/10.1111/j.1365-3156.2007.01939.x
Julshamn K, Nilsen BM, Frantzen S, Valdersnes S, Maage A, Nedreaas K, Sloth JJ (2012) Total and inorganic arsenic in fish samples from Norwegian waters. Food Addit Contam Part B Surveill 5:229–235. https://doi.org/10.1080/19393210.2012.698312
Ling MP, Wu CH, Chen SC, Chen WY, Chio CP, Cheng YH, Liao CM (2014) Probabilistic framework for assessing the arsenic exposure for assessing the arsenic exposure risk from cooked fish consumption. Environ Geochem Health 36:1115–1128. https://doi.org/10.1007/s10653-014-9621-8
Pei J, Zuo J, Wang X, Yin J, Liu L, Fan W (2019) The bioaccumulation and tissue distribution of arsenic species in Tilapia. Int J Environ Res Public Health 16:757. https://doi.org/10.3390/ijerph16050757
Choi SD, Son HS, Choi M, Park MK (2015) Accumulation features of arsenic species in various fishes collected from coastal cities in Korea. Ocean Sci J 50:741–750. https://doi.org/10.1007/s12601-015-0066-5
Culioli JL, Calendini S, Mori C, Orsini A (2009) Arsenic accumulation in a freshwater fish living in a contaminated river of Corsica, France. Ecotox Environ Safety 72:1440–1445. https://doi.org/10.1016/j.ecoenv.2009.03.003
Ibrahem MD (2015) Evolution of probiotics in aquatic world: potential effects, the current status in Egypt and recent prospective. J Adv Res 6:765–791. https://doi.org/10.1016/j.jare.2013.12.004
Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei M (2012) Characterization of lactic acid bacteria-based probiotics as heavy metals sorbents. J Appl Microbiol 112:1193–1206. https://doi.org/10.1111/j.1365-2672.2012.05284.x
Macey BM, Coyne VE (2005) Improved growth rate and disease resistance of farmed Haliotismidae through probiotic treatment. Aquaculture 245:249–261. https://doi.org/10.1016/j.aquaculture.2004.11.031
Bandyopadhyay P, Das Mohapatra PK (2009) Effect of a probiotic bacterium Bacillus circulans PB7 in the formulated diets: on growth, nutritional quality and immunity of Catla catla (Ham.). Fish Physiol Biochem 35(3):467–478. https://doi.org/10.1007/s10695-008-9272-8
Sugita H, Ishigaki T, Iwai D, Suzuki Y, Okano R, Matsuura S, Asfie M, Aono E, Deguchi Y (1998) Antibacterial abilities of intestinal bacteria from three coastal fishes. Suisan Zoshoku 46:563–568
Panigrahi A, Kiron V, Puangkaew J, Kobayashi T, Satoh S, Sugita H (2004) The viability of probiotic bacteria as a factor influencing the immune response in rainbow trout Oncorhynchus mykiss. Aquaculture 243:241–254. https://doi.org/10.1016/j.aquaculture.2004.09.032
Daya U, Chatterjeeb S, Mondala NK (2016) Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnol Rep 10:1–7. https://doi.org/10.1016/j.btre.2016.02.002
Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K (2010) Isolation and probiotic characterization of arsenic-resistant lactic acid bacteria for uptaking arsenic. International J Chem Biol Eng 3:167–174. https://doi.org/10.5281/zenodo.1083023
Bhakta JN, Lahiri S, Bhuiyna FA, Rokunuzzaaman Md, Ohonishi K, Iwasaki K, Jana BB (2018) Profiling of heavy metal(loid)-resistant bacterial community structure by metagenomic-DNA fingerprinting using PCR–DGGE for monitoring and bioremediation of contaminated environment. Energ Ecol Environ 3:102–109. https://doi.org/10.1007/s40974-017-0079-2
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. https://doi.org/10.1016/j.ijfoodmicro.2006.10.040
Elsanhoty RM, Al-Turki IA, Ramadan MF (2016) Application of lactic acid bacteria in removing heavy metals and aflatoxin B1 from contaminated water. Water Sci Technol 74:625–638. https://doi.org/10.2166/wst.2016.255
Coryell M, McAlpine M, Pinkham NV, Mc Dermott TR, Walk ST (2018) The gut microbiome is required for full protection against acute arsenic toxicity in mouse models. Nat Commun 9:5424. https://doi.org/10.1038/s41467-018-07803-9
Thornton I, Butler D, Docx P, Hession M, Makropoulos C, McMullen M, Nieuwenhuijsen M, Pitman A, Rautiu R, Sawyer R, Smith S, White D, Wilderer P, Paris S, Marani D, Braguglia C, Palerm J (2001) Pollutants in urban wastewater and sewage sludge. Report prepared by ICON, IC Consultants Ltd, UK for the European Commission, Luxembourg
Zhang X, Wang X-q, Wang D-f (2017) Immobilization of heavy metals in sewage sludge during land application process in China: a review. Sustainability 9. https://doi.org/10.3390/su9112020
Giller K, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414. https://doi.org/10.1016/S0038-0717(97)00270-8
Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46:834–840. https://doi.org/10.1007/BF01935534
Idris R, Trifonova R, Puschenreiter M (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677. https://doi.org/10.1128/AEM.70.5.2667-2677.2004
Solovyev MM, Kashinskaya EN, Izvekova GI, Glupov VV (2015) pH values and activity of digestive enzymes in the gastrointestinal tract of fish in Lake Chany (West Siberia). J Ichthyol 55:251–258. https://doi.org/10.1134/S0032945215010208
Yu´fera M, Moyano FJ, Astola A, Pousao-Ferreira P, Martinez-Rodriguez G (2012) Acidic digestion in a teleost: postprandial and circadian pattern of gastric pH, pepsin activity, and pepsinogen and proton pump mRNAs expression. PLoS One 7(3):e33687. https://doi.org/10.1371/journal.pone.0033687
Aas TS, Sixten HJ, Hillestad M, Sveier H, Ytrestøy T, Hatlena H, Åsgård T (2017) Measurement of gastrointestinal passage rate in Atlantic salmon (Salmo salar) fed dry or soaked feed. Aquac Rep 8:49–57. https://doi.org/10.1016/j.aqrep.2017.10.001
Abidin DAZ, Hashim M, Das SK, Rahim SM, Mazlan AG (2016) Enzymatic digestion of stomachless fish Zenarchopterus buffonis. AACL Bioflux 9:695–703
Honkanen RE, Rigler MW, Patton JS (1985) Dietary fat assimilation and bile salt absorption in the killifish intestine. Am J Physiol G399–G407. https://doi.org/10.1152/ajpgi.1985.249.3.G399
Balca´zar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz JL, Girones O (2008) Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 278:188–191. https://doi.org/10.1016/j.aquaculture.2008.03.014
Ruiz-Barba JL, Maldonado A, Jiménez Díaz R (2005) Small-scale total DNA extraction from bacteria and yeast for PCR applications. Anal Biochem 347:333–335. https://doi.org/10.1016/j.ab.2005.09.028
Wheelis M (2008) Principles of modern microbiology. Jones & Bartlett Publishers, Inc., Sudbury. Am Soc Microbiol
Reiner K (2016) Catalase test protocol. Am Soci Microbiol. www.asmscience.org
Mahon CR, Lehman DC, Manuselis G (2011) Text book of diagnostic microbiology, 4th edn. W.B. Saunders Co., Philadelphia, PA
Pennacchia C, Ercolini D, Blaiotta G, Pepe O, Mauriello F, Villani F (2004) Selection of Lactobacillus strains from fermented sausages for their potential use as probiotics. Meat Sci 67:309–317. https://doi.org/10.1016/j.meatsci.2003.11.003
Kapoor BB, Smit H, Verighina IA (1975) The alimentary canal and digestion in teleosts. Adv Mar Biol 13:109–239. https://doi.org/10.1016/S0065-2881(08)60281-3
Solovyev MM, Kashinskaya E, Izvekova G, Glupov VV (2015) pH values and activity of digestive enzymes in the gastrointestinal tract of fish in Lake Chany (West Siberia). J Ichthyol 55:251–258. https://doi.org/10.1134/S0032945215010208
Zhang Z, Xing T, Dapeng LI (2016) Tissue pH and gut ecomorphology in six freshwater teleosts occupying different trophic levels. Turk J Zool 40:713–719. https://doi.org/10.3906/zoo-1511-5
Erkkila S, Petaja E (2000) Screening of commercial meat starter cultures at low pH in the presence of bile salts for potential probiotic use. Meat Sci 55:297–300. https://doi.org/10.1016/s0309-1740(99)00156-4
Smith LS (1980) Digestion in teleost fish. In Lectures presented at the FAO/UNPD training course in fish feed technology. ADCP/REP/80/11, 3–17. http://www.fao.org/3/x5738e/x5738e02.htm
Gilliland S, Staley T, Bush L (1984) Importance of bile tolerance of Lactobacillus acidophilus used as dietary adjunct. J Dairy Sci 67:3045–3051. https://doi.org/10.3168/jds.S0022-0302(84)81670-7
Goldin B, Gorbach S (1992) Probiotics for humans. In Fuller R, Probiotics- the scientific basis, London. Chapman and Hall pp 355–376. https://doi.org/10.1007/978-94-011-2364-8_13
Midhun SJ, Neethu S, Vysakh A, Arun D, Radhakrishnan EK (2017) Jyothis M. Antibacterial activity and probiotic characterization of autochthonous Paenibacillus polymyxa isolated from Anabas testudineus. Microb Pathog 113:403–411. https://doi.org/10.1016/j.micpath.2017.11.019
Karimi S, Azizi F, Aghaee MN, Mahmoodnia L (2018) The antimicrobial activity of probiotic bacteria Escherichia coli isolated from different natural sources against hemorrhagic, E. coli O157:H7. Electron Physician 10:6548–6553. https://doi.org/10.19082/6548
Mirzaei EZ, Lashani E, Davoodabad A (2018) Antimicrobial properties of lactic acid bacteria isolated from traditional yogurt and milk against Shigella strains. GMS Hyg Infect Control 13:1–5. https://doi.org/10.3205/dgkh000307
Alvarado C, Garcia ABE, Martin SE, Regalado C (2006) Food-associated lactic acid bacteria with antimicrobial potential from traditional Mexican foods. Revista Latino Microbiol 48:260–268
Sorrells KM, Speck ML (1970) Inhibition of Salmonella gallinarum by culture filtrates of Leuconostoc citrovorum. J Dairy Sci 53:239–241. https://doi.org/10.3168/jds.S0022-0302(70)86186-0
Hwanhlem N, Watthanasakphuban N, Riebroy S, Benjakul S, Kittikun AH, Maneerat S (2010) Probiotic lactic acid bacteria from Kung-Som: isolation, screening, inhibition of pathogenic bacteria. Int J Food Sci Technol 45:594–601. https://doi.org/10.1111/j.1365-2621.2010.02172.x
Gonzalez L, Sandoval H, Sacristan N, Castro JM, Fresno JM, Tornadijo ME (2007) Identification of lactic acid bacteria isolated from Genestoso cheese throughout ripening and study of their antimicrobial activity. Food Control 18:716–722. https://doi.org/10.1016/j.foodcont.2006.03.008
Prasad N, Tripathi M, Shukla S, Ramteke W, Chandra R (2005) Functional properties of heavy metal tolerant probiotic strains isolated from Curd. Ann Res Rev Biol 28:1–11. https://doi.org/10.9734/ARRB/2018/43480
Qing H, Min-Na D, Hong-Yan D, Xiang-Ming X, Guo-Qiang Z, Min Y (2007) Detection, isolation, and identification of cadmium-resistant bacteria based on PCR-DGGE. J Environ Sci 19:1114–1119. https://doi.org/10.1016/s1001-0742(07)60181-8
Foster TJ (1983) Plasmid determined resistance to antimicrobial drugs and toxic metal ions in bacteria. Microbiol Rev 47:361–409. https://doi.org/10.1128/mr.47.3.361-409.1983
Kirillova AV, Danilushkina AA, Irisov DS, Bruslik NL, Fakhrullin RF, Zakharov YA, Bukhmin VS, Yarullina DR (2017) Assessment of resistance and bioremediation ability of Lactobacillus Strains to Lead and Cadmium. Int J Microbiol 7:9869145. https://doi.org/10.1155/2017/9869145
Feng P, Ze Ye, Kakade A, Virk AK, Li X, Liu P (2018) A review on gut remediation of selected environmental contaminants: possible roles of probiotics and gut microbiota. Nutrients 11:1–19. https://doi.org/10.3390/nu11010022
Bhakta JN (2016) Microbial response against metal toxicity. In Rathoure AK, Dhatwalia VK (eds) Toxicity and waste management using bioremediation, IGI Global, PA, USA, pp 75–96. https://doi.org/10.4018/978-1-4666-9734-8.ch004
Wong A, Ngu DYS, Dan LA, Amanda O, Lim RLH (2016) Detection of antibiotic resistance in probiotics of dietary supplements. Nutrition J 14:1–6. https://doi.org/10.1186/s12937-015-0084-2
Trinder M, McDowell TW, Daisley BA, Ali SN, Leong HS, Sumarah MW, Reid G (2016) Probiotic Lactobacillus rhamnosus reduces organophosphate pesticide absorption and toxicity to Drosophila melanogaster. Appl Environ Microbiol 82:6204–6213. https://doi.org/10.1128/AEM.01510-16
Vieira GRADS, Soares M, Ramírez NCB, Schleder DD, Silv BCD, Mouriño JLP, Andreatta ER, Vieira FDN (2016) Lactic acid bacteria used as preservative in fresh feed for marine shrimp maturation. Pesq Agropec Bras Brasília 51:1799–1805. https://doi.org/10.1590/S0100-204X2016001100001
Vieira FDN, Pedrotti FS, Neto CCB, Mouriño JLP, Beltrame E, Martins ML, Ramirez C, Arana LAV (2007) Lactic-acid bacteria increase the survival of marine shrimp, Litopenaeus vannamei, after infection with Vibrio harveyi. Braz J Oceanogr 55:251–255
Vieira FDN, Jatobá A, Mouriño JLP, Vieira EA, Soares M, Silva W, Seiffert Q, Martins ML, Vinatea LA (2013) In vitro selection of bacteria with potential for use as probiotics in marine shrimp culture. Pesq Agrop Brasileira 48:998–1004. https://doi.org/10.1590/S0100-204X2013000800027
Kanmani P, Satish RK, Yuvaraj K, Paari A, Pattukumar V, Arul V (2013) Probiotics and its functionally valuable products-a review. Crit Rev Food Sci Nutr 53:641–658. https://doi.org/10.1080/10408398.2011.553752
Acknowledgements
All the co-investigators and authors are thankful to DHESTB for sponsoring the grant.
Funding
This study is supported by a research grant (No. 237(Sanc.)/ST/P/S&T/1G-12/2017) from the Department of Higher Education, Science & Technology and Biotechnology (DHESTB), Government of West Bengal to JNB.
Author information
Authors and Affiliations
Contributions
JNB conceived the research idea, received the research grant, carried out the research work, analysed the samples, processed the results and wrote the first draft of the manuscript. SB helped to conduct the experiments and collect the sample and data. SL contributed to analysing the results. AKP reviewed the first draft of the manuscript.
Corresponding author
Ethics declarations
Ethics Approval
The present research did not include any human subjects and animal experiments.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
12602_2022_9921_MOESM1_ESM.docx
Supplementary file1 Bacterial cultured plate showing both yellow coloured pronouncing and non-yellow coloured pronouncing bacterial colonies (DOCX 518 KB)
12602_2022_9921_MOESM2_ESM.docx
Supplementary file2 The profile of catalase activity of 51 isolates, morphological study of selected 22 CNIs, gastric enzyme and acid pH tolerance of selected 22 CNIs and intestinal enzyme and bile salt tolerance of selected 10 GEATIs. Six IEBTIs successfully passed through the different mimic gastrointestinal conditions, therefore, 6 IEBTIs were considered as potential probiotic candidates (in catalase test, + = catalase positive and - = catalase negative; in the test of “Gastric enzyme and acid pH tolerance” and “Intestinal enzyme and bile salt tolerance”, + = viable and - = not viable) (DOCX 17 KB)
Rights and permissions
About this article
Cite this article
Bhakta, J.N., Bhattacharya, S., Lahiri, S. et al. Probiotic Characterization of Arsenic-resistant Lactic Acid Bacteria for Possible Application as Arsenic Bioremediation Tool in Fish for Safe Fish Food Production. Probiotics & Antimicro. Prot. 15, 889–902 (2023). https://doi.org/10.1007/s12602-022-09921-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-022-09921-9