Abstract
Mercury (Hg) is a global pollutant, which is linked with different diseases. The methylation of Hg and demethylation of methylmercury (MeHg) in the environment were extensively studied and summarized; however, the transformation of Hg in the intestine is less presented. In this review, the research progress and the perspectives on the intestinal transformation of Hg were discussed. Studies found that MeHg could be formed when exposed to inorganic Hg by the gut microbiota in aquatic organisms, terrestrial invertebrates, and mammals, etc. hgcAB genes could be used as indicators for predicting Hg methylation potential. In vitro studies using fecal specimen, intestinal contents, and the isolated intestinal microbes confirmed the intestinal demethylation of MeHg. The investigation on the effects of Hg exposure to the abundance and diversity of intestinal microbes and their metabolites could shed light on the mechanism of the toxicity of Hg, especially the neurotoxicity of MeHg, which deserves further study.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdulla M, Arnesjo B, Ihse I (1973) Methylation of inorganic mercury in experimental jejunal blind-loop. Scand J Gastroent 8:565–567
Baldi F, Parati F, Filippelli M (1995) Dimethylmercury and dimethylmercury-sulfide of microbial origin in the biogeochemical cycle of Hg. Water Air Soil Pollut 80:805–815. https://doi.org/10.1007/BF01189732
Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384. https://doi.org/10.1016/s0168-6445(03)00046-9
Beerens H, Romond C (1977) Sulfate-reducing anaerobic bacteria in human feces. Am J Clin Nutr 30:1770–1776
Blander JM, Longman RS, Iliev ID, Sonnenberg GF, Artis D (2017) Regulation of inflammation by microbiota interactions with the host. Nat Immunol 18:851. https://doi.org/10.1038/ni.3780
Bloom NS (1992) On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 49:1010–1017. https://doi.org/10.1139/f92-113
Brown GG (1995) How do earthworms affect microfloral and faunal community diversity? Plant Soil 170:209–231. https://doi.org/10.1007/bf02183068
Brun A, Abdulla M, Ihse I, Samuelsson B (1976) Uptake and localization of mercury in the brain of rats after prolonged oral feeding with mercuric chloride. Histochemistry 47:23
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563. https://doi.org/10.1038/nature12820
Deacon GB (1978) Volatilization of methylmercuric chloride by hydrogen sulphide. Nature 275:344–344
Edwards T, Mcbride BC (1975) Biosynthesis and degradation of methylmercury in human faeces. Nature 253:463
Feng X, Li P, Qiu G, Wang S, Li G, Shang L, Meng B, Jiang H, Bai W, Li Z, Fu X (2008) Human exposure to methylmercury through rice intake in mercury mining areas, Guizhou province, China. Environ Sci Technol 42:326–332. https://doi.org/10.1021/es071948x
Fröhlich J, Sass H, Babenzien H-D, Kuhnigk T, Varma A, Saxena S, Nalepa C, Pfeiffer P, König H (1999) Isolation of Desulfovibrio intestinalis sp. nov. from the hindgut of the lower termite Mastotermes darwiniensis. Can J Microbiol 45:145–152. https://doi.org/10.1139/w98-222
Fung TC, Olson CA, Hsiao EY (2017) Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 20:145–155. https://doi.org/10.1038/nn.4476
Furutani A, Rudd JWM (1980) Measurement of mercury methylation in lake water and sediment samples. Appl Environ Microbiol 40:770–776
Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD, Somenahally AC, Johs A, Hurt RA, Bailey KL, Elias DA (2013) Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810–11820. https://doi.org/10.1021/es403075t
Girard C, Charette T, Leclerc M, Shapiro BJ, Amyot M (2018) Cooking and co-ingested polyphenols reduce in vitro methylmercury bioaccessibility from fish and may alter exposure in humans. Sci Total Environ 616–617:863–874. https://doi.org/10.1016/j.scitotenv.2017.10.236
Gu C, Xu H, Qiu G (2013) The progress in research on mechanism of microbial mercury methylation and de-methylation. Environ Chem 32:926–936
Guarner F, Malagelada J-R (2003) Gut flora in health and disease. Lancet 361:512–519. https://doi.org/10.1016/S0140-6736(03)12489-0
Hall B, Bloom NS, Munthe J (1995) An experimental study of two potential methylation agents of mercury in the atmosphere: CH3I and DMS. Water Air Soil Pollut 80:337–341. https://doi.org/10.1007/bf01189683
He Q, Xing Z, Zhang S, Zhang X (2015) ICP-MS/MS as a tool to study abiotic methylation of inorganic mercury reacting with VOCs. J Anal Atom Spectrom 30:1997–2002. https://doi.org/10.1039/C5JA00245A
Horvat M, Nolde N, Fajon V, Jereb V, Logar M, Lojen S, Jacimovic R, Falnoga I, Qu L, Faganeli J (2003) Total mercury, methylmercury and selenium in mercury polluted areas in the province Guizhou, China. Sci Total Environ 304:231–256
Howie MG, Jackson AK, Cristol DA (2018) Spatial extent of mercury contamination in birds and their prey on the floodplain of a contaminated river. Sci Total Environ 630:1446–1452. https://doi.org/10.1016/j.scitotenv.2018.02.272
Hsu-Kim H, Kucharzyk KH, Zhang T, Deshusses MA (2013) Mercury bioavailability for methylating microorganisms in the aquatic environment: a critical review. Environ Sci Technol 47:2441–2456. https://doi.org/10.1021/es304370g
Jadán-Piedra C, Alcántara C, Monedero V, Zúñiga M, Vélez D, Devesa V (2017) The use of lactic acid bacteria to reduce mercury bioaccessibility. Food Chem 228:158–166. https://doi.org/10.1016/j.foodchem.2017.01.157
Jadán-Piedra C, Vélez D, Devesa V (2018) In vitro evaluation of dietary compounds to reduce mercury bioavailability. Food Chem 248:353–359. https://doi.org/10.1016/j.foodchem.2017.12.012
Jensen S, Jernelöv A (1969) Biological methylation of mercury in aquatic organisms. Nature 223:753–754. https://doi.org/10.1038/223753a0
Jereb V, Horvat M, Drobne D, Pihlar B (2003) Transformations of mercury in the terrestrial isopod Porcellio scaber (Crustacea). Sci Total Environ 304:269–284. https://doi.org/10.1016/S0048-9697(02)00574-0
Kaschak E, Knopf B, Petersen JH, Bings NH, König H (2014) Biotic methylation of mercury by intestinal and sulfate-reducing bacteria and their potential role in mercury accumulation in the tissue of the soil-living Eisenia foetida. Soil Biol Biochem 69:202–211. https://doi.org/10.1016/j.soilbio.2013.11.004
Khan MAK, Wang F (2010) Chemical demethylation of methylmercury by selenoamino acids. Chem Res Toxicol 23:1202–1206. https://doi.org/10.1021/tx100080s
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. https://doi.org/10.1016/j.resmic.2013.04.004
Kostanjšek R, Lapanje A, Rupnik M, Štrus J, Drobne D, Avguštin G (2004) Anaerobic bacteria in the gut of terrestrial isopod crustacean Porcellio scaber. Folia Microbiol 49:179–182. https://doi.org/10.1007/bf02931397
Kozak S, Forsberg CW (1979) Transformation of mercuric chloride and methylmercury by the rumen microflora. Appl Environ Microbiol 38:626–636
Landry TD, Doherty RA, Gates AH (1979) Effects of three diets on mercury excretion after methylmercury administration. Bull Environ Contam Toxicol 22:151–158. https://doi.org/10.1007/bf02026922
Lapanje A, Zrimec A, Drobne D, Rupnik M (2010) Long-term Hg pollution-induced structural shifts of bacterial community in the terrestrial isopod (Porcellio scaber) gut. Environ Pollut 158:3186–3193. https://doi.org/10.1016/j.envpol.2010.07.001
Li Y, Cai Y (2013) Progress in the study of mercury methylation and demethylation in aquatic environments. Chin Sci Bull 58:177–185. https://doi.org/10.1007/s11434-012-5416-4
Li Y, Zhao J, Guo J, Liu M, Xu Q, Li H, Li Y-F, Zheng L, Zhang Z, Gao Y (2017) Influence of sulfur on the accumulation of mercury in rice plant (Oryza sativa L.) growing in mercury contaminated soils. Chemosphere 182:293–300. https://doi.org/10.1016/j.chemosphere.2017.04.129
Limper U, Knopf B, König H (2008) Production of methyl mercury in the gut of the Australian termite Mastotermes darwiniensis. J Appl Entomol 132:168–176
Lin H, Lu X, Liang L, Gu B (2015) Cysteine inhibits mercury methylation by Geobacter sulfurreducens PCA mutant ∆omcBESTZ. Environ Sci Technol Lett 2:144–148. https://doi.org/10.1021/acs.estlett.5b00068
Liu Y-R, Yu R-Q, Zheng Y-M, He J-Z (2014) Analysis of the microbial community structure by monitoring an Hg methylation gene (hgcA) in paddy soils along an Hg gradient. Appl Environ Microbiol 80:2874–2879. https://doi.org/10.1128/aem.04225-13
Liu Y-R, Delgado-Baquerizo M, Bi L, Zhu J, He J-Z (2018a) Consistent responses of soil microbial taxonomic and functional attributes to mercury pollution across China. Microbiome 6:183. https://doi.org/10.1186/s40168-018-0572-7
Liu Y-R, Johs A, Bi L, Lu X, Hu H-W, Sun D, He J-Z, Gu B (2018b) Unraveling microbial communities associated with methylmercury production in paddy soils. Environ Sci Technol 52:13110–13118. https://doi.org/10.1021/acs.est.8b03052
Lu X, Liu Y, Johs A, Zhao L, Wang T, Yang Z, Lin H, Elias DA, Pierce EM, Liang L, Barkay T, Gu B (2016) Anaerobic mercury methylation and demethylation by Geobacter bemidjiensis Bem. Environ Sci Technol 50:4366–4373. https://doi.org/10.1021/acs.est.6b00401
Lu X, Gu W, Zhao L, Farhan Ul Haque M, DiSpirito AA, Semrau JD, Gu B (2017) Methylmercury uptake and degradation by methanotrophs. Sci Adv 3:e1700041–e1700041. https://doi.org/10.1126/sciadv.1700041
Ludwicki JK (1989) Studies on the role of gastrointestinal tract contents in the methylation of inorganic mercury compounds. Bull Environ Contam Toxicol 42:283–288. https://doi.org/10.1007/bf01699412
Martín-Doimeadios RCR, Mateo R, Jiménez-Moreno M (2017) Is gastrointestinal microbiota relevant for endogenous mercury methylation in terrestrial animals? Environ Res 152:454–461. https://doi.org/10.1016/j.envres.2016.06.018
Marvin-DiPasquale MC, Oremland RS (1998) Bacterial methylmercury degradation in Florida Everglades peat sediment. Environ Sci Technol 32:2556–2563. https://doi.org/10.1021/es971099l
Mostafa GA, AL-Ayadhi LY (2015) The possible association between elevated levels of blood mercury and the increased frequency of serum anti-myelin basic protein auto-antibodies in autistic children. J Clin Cell Immunol 6:310. https://doi.org/10.4172/2155-9899.1000310
Nakamura I, Hosokawa K, Tamura H, Miura T (1977) Reduced mercury excretion with feces in germfree mice after oral administration of methyl mercury chloride. Bull Environ Contam Toxicol 17:528–533. https://doi.org/10.1007/bf01685974
Nierenberg DW, Nordgren RE, Chang MB, Siegler RW, Blayney MB, Hochberg F, Toribara TY, Cernichiari E, Clarkson T (1998) Delayed cerebellar disease and death after accidental exposure to dimethylmercury. N Engl J Med 338:1672–1676. https://doi.org/10.1056/nejm199806043382305
Norseth T, Clarkson TW (1970) Studies on the biotransformation of 203Hg-labeled methyl mercury chloride in rats. Arch Environ Health 21:717–727. https://doi.org/10.1080/00039896.1970.10667325
Oremland RS, Culbertson CW, Winfrey MR (1991) Methylmercury decomposition in sediments and bacterial cultures: involvement of methanogens and sulfate reducers in oxidative demethylation. Appl Environ Microbiol 57:130–137
Pan-Hou HSK, Imura N (1981) Biotransformation of mercurials by intestinal microorganisms isolated from yellowfin tuna. Bull Environ Contam Toxicol 26:359–363. https://doi.org/10.1007/BF01622102
Parks JM, Johs A, Podar M, Bridou R, Hurt RA, Smith SD, Tomanicek SJ, Qian Y, Brown SD, Brandt CC, Palumbo AV, Smith JC, Wall JD, Elias DA, Liang L (2013) The genetic basis for bacterial mercury methylation. Science 339:1332–1335. https://doi.org/10.1126/science.1230667
Patiño Ropero MJ, Rodríguez Fariñas N, Mateo R, Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC (2016) Mercury species accumulation and trophic transfer in biological systems using the Almadén mining district (Ciudad Real, Spain) as a case of study. Environ Sci Pollut Res 23:6074–6081. https://doi.org/10.1007/s11356-015-4989-2
Pennacchioni A, Marchetti R, Gaggino GF (1976) Inability of fish to methylate mercuric chloride in vivo. J Environ Qual 5:451–454. https://doi.org/10.2134/jeq1976.00472425000500040027x
Podar M, Gilmour CC, Brandt CC, Soren A, Brown SD, Crable BR, Palumbo AV, Somenahally AC, Elias DA (2015) Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci Adv 1:e1500675. https://doi.org/10.1126/sciadv.1500675
Rao M, Gershon MD (2016) The bowel and beyond: the enteric nervous system in neurological disorders. Nat Rev Gastroenterol Hepatol 13:517–528. https://doi.org/10.1038/nrgastro.2016.107
Rieder SR, Brunner I, Horvat M, Jacobs A, Frey B (2011) Accumulation of mercury and methylmercury by mushrooms and earthworms from forest soils. Environ Pollut 159:2861–2869. https://doi.org/10.1016/j.envpol.2011.04.040
Rieder SR, Brunner I, Daniel O, Liu B, Frey B (2013) Methylation of mercury in earthworms and the effect of mercury on the associated bacterial communities. PLoS ONE 8:e61215. https://doi.org/10.1371/journal.pone.0061215
Rodríguez Álvarez C, Jiménez Moreno M, Guzmán Bernardo FJ, Rodríguez Martín-Doimeadios RC, Berzas Nevado JJ (2014) Mercury methylation, uptake and bioaccumulation by the earthworm Lumbricus terrestris (Oligochaeta). Appl Soil Ecol 84:45–53. https://doi.org/10.1016/j.apsoil.2014.06.008
Rothenberg SE, Keiser S, Ajami NJ, Wong MC, Gesell J, Petrosino JF, Johs A (2016) The role of gut microbiota in fetal methylmercury exposure: insights from a pilot study. Toxicol Lett 242:60–67. https://doi.org/10.1016/j.toxlet.2015.11.022
Rowland IR, Grasso P, Davies MJ (1975) The methylation of mercuric chloride by human intestinal bacteria. Experientia 31:1064–1065
Rowland IR, Davies MJ, Grasso P (1977) Volatilisation of methylmercuric chloride by hydrogen sulphide. Nature 265:718–719
Rowland IR, Davies MJ, Grasso P (1978) Metabolism of methylmercuric chloride by the gastro-intestinal flora of the rat. Xenobiotica 8:37–43
Rowland IR, Davies MJ, Evans JG (1980) Tissue content of mercury in rats given methylmercuric chloride orally: influence of intestinal flora. Arch Environ Health 35:155–160. https://doi.org/10.1080/00039896.1980.10667485
Rowland IR, Robinson RD, Doherty RA, Landry TD (1983) Are developmental changes in methylmercury metabolism and excretion mediated by the intestinal microflora? In: Clarkson TW, Nordberg GF, Sager PR (eds) Reproductive and developmental toxicity of metals. Springer, Boston, pp 745–758. https://doi.org/10.1007/978-1-4615-9346-1_32
Rowland IR, Robinson RD, Doherty RA (1984) Effects of diet on mercury metabolism and excretion in mice given methylmercury: role of gut flora. Arch Environ Health 39:401–408. https://doi.org/10.1080/00039896.1984.10545872
Rowland IR, Mallett AK, Flynn J, Hargreaves RJ (1986) The effect of various dietary fibres on tissue concentration and chemical form of mercury after methylmercury exposure in mice. Arch Toxicol 59:94–98. https://doi.org/10.1007/BF00286730
Rudd J, Furutani A, Turner MA (1980) Mercury methylation by fish intestinal contents. Appl Environ Microbiol 40:777–782
Sakamoto M, Yasutake A, Kakita A, Ryufuku M, Chan HM, Yamamoto M, Oumi S, Kobayashi S, Watanabe C (2013) Selenomethionine protects against neuronal degeneration by methylmercury in the developing rat cerebrum. Environ Sci Technol 47:2862–2868. https://doi.org/10.1021/es304226h
Sun J, Chen C, Li B, Li Y-F, Wang J, Gao Y, Chai Z (2006) Analysis of total mercury and methylmercury concentrations in four commercially important freshwater fish species obtained from Beijing markets. J Hyg Res 11:722–725
Sun R, Wang D, Zhang Y, Mao W, Zhang T, Ma M, Zhang C (2013) Photo-degradation of monomethylmercury in the presence of chloride ion. Chemosphere 91:1471–1476. https://doi.org/10.1016/j.chemosphere.2012.12.013
Tai C, Li Y, Yin Y, Scinto LJ, Jiang G, Cai Y (2014) Methylmercury photodegradation in surface water of the Florida Everglades: importance of dissolved organic matter-methylmercury complexation. Environ Sci Technol 48:7333–7340. https://doi.org/10.1021/es500316d
Trinkerl M, Breunig A, Schauder R, König H (1990) Desulfovibrio termitidis sp. nov., a carbohydrate-degrading sulfate-reducing bacterium from the hindgut of a termite. Syst Appl Microbiol 13:372–377. https://doi.org/10.1016/S0723-2020(11)80235-3
Trust TJ, Bull LM, Currie BR, Buckley JT (1979) Obligate anaerobic bacteria in the gastrointestinal microflora of the grass carp (Ctenopharyngodon idella), goldfish (Carassius auratus), and rainbow trout (Salmo gairdneri). J Fish Res Board Can 36:1174–1179
Wang R, Feng X-B, Wang W-X (2013) In vivo mercury methylation and demethylation in freshwater tilapia quantified by mercury stable isotopes. Environ Sci Technol 47:7949–7957. https://doi.org/10.1021/es3043774
Wang Y-j, Dang F, Zhao J-t, Zhong H (2016) Selenium inhibits sulfate-mediated methylmercury production in rice paddy soil. Environ Pollut 213:232–239. https://doi.org/10.1016/j.envpol.2016.02.021
Xu X, Zhao J, Li Y, Fan Y, Zhu N, Gao Y, Li B, Liu H, Li Y-F (2016) Demethylation of methylmercury in growing rice plants: an evidence of self-detoxification. Environ Pollut 210:113–120. https://doi.org/10.1016/j.envpol.2015.12.013
Yin Y, Li Y, Tai C, Cai Y, Jiang G (2014) Fumigant methyl iodide can methylate inorganic mercury species in natural waters. Nat Commun 5:4633. https://doi.org/10.1038/ncomms5633
Zhang Y, Liu Y-R, Lei P, Wang Y-J, Zhong H (2018) Biochar and nitrate reduce risk of methylmercury in soils under straw amendment. Sci Total Environ 619–620:384–390. https://doi.org/10.1016/j.scitotenv.2017.11.106
Funding
Fundings were provided by National Natural Science Foundation of China with Grant No. 11475196 and Ministry of Science and Technology of the People's Republic of China with Grant No. 2016YFA0201600.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, H., Lin, X., Zhao, J. et al. Intestinal Methylation and Demethylation of Mercury. Bull Environ Contam Toxicol 102, 597–604 (2019). https://doi.org/10.1007/s00128-018-2512-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-018-2512-4