Abstract
The interactions and mechanisms between sulfur and heavy metals are a growing focus of biogeochemical studies in coastal wetlands. These issues underline the fate of heavy metals bound in sediments or released into the system through sediments. Despite the fact that numerous published studies have suggested sulfur has a significant impact on the bioavailability of heavy metals accumulated in coastal wetlands, to date, no review article has systematically summarized those studies, particularly from the perspective of the three major components of wetland ecosystems (sediments, rhizosphere, and vegetation). The present review summarizes the studies published in the past four decades and highlights the major achievements in this field. Research and studies available thus far indicate that under anaerobic conditions, most of the potentially bioavailable heavy metals in coastal wetland sediments are fixed as precipitates, such as metal sulfides. However, fluctuations in physicochemical conditions may affect sulfur cycling, and hence, directly or indirectly lead to the conversion and migration of heavy metals. In the rhizosphere, root activities and microbes together affect the speciation and transformation of sulfur which in turn mediate the migration of heavy metals. As for plant tissues, tolerance to heavy metals is enhanced by sulfur-containing compounds via promoting a series of chelation and detoxification processes. Finally, to further understand the interactions between sulfur and heavy metals in coastal wetlands, some major future research directions are proposed.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Ali B, Gill R A, Yang S, Gill M B, Ali S, Rafiq M T, Zhou W (2014). Hydrogen sulfide alleviates cadmium-induced morpho-physiological and ultrastructural changes in Brassica napus. Ecotoxicology and Environmental Safety, 110: 197–207
Allen H E, Fu G, Deng B (1993). Analysis of acid-volatile sulfide (AVS) and simultaneously extracted metals (SEM) for the estimation of potential toxicity in aquatic sediments. Environmental Toxicology and Chemistry, 12(8): 1441–1453
Alongi D M (2010). Dissolved iron supply limits early growth of estuarine mangroves. Ecology, 91(11): 3229–3241
Arfaeinia H, Nabipour I, Ostovar A, Asadgol Z, Abuee E, Keshtkar M, Dobaradaran S (2016). Assessment of sediment quality based on acid-volatile sulfide and simultaneously extracted metals in heavily industrialized area of Asaluyeh, Persian Gulf: Concentrations, spatial distributions, and sediment bioavailability/toxicity. Environmental Science and Pollution Research International, 23(10): 9871–9890
Ashraf U, Kanu A S, Mo Z, Hussain S, Anjum S A, Khan I, Abbas R N, Tang X (2015). Lead toxicity in rice: effects, mechanisms, and mitigation strategies: A mini review. Environmental Science and Pollution Research International, 22(23): 18318–18332
Barton L L, Fauque G D (2009). Advances in Applied Microbiology. New York: Academic Press, 41–98
Bonanno G, Lo Giudice R (2010). Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecological Indicators, 10(3): 639–645
Cao Z Z, Qin M L, Lin X Y, Zhu Z W, Chen M X (2018). Sulfur supply reduces cadmium uptake and translocation in rice grains (Oryza sativa L.) by enhancing iron plaque formation, cadmium chelation and vacuolar sequestration. Environmental Pollution, 238: 76–84
Chai M, Shen X, Li R, Qiu G (2015). The risk assessment of heavy metals in Futian mangrove forest sediment in Shenzhen Bay (South China) based on SEM-AVS analysis. Marine Pollution Bulletin, 97 (1–2): 431–439
Chai M, Shi F, Li R, Liu F, Qiu G, Liu L (2013). Effect of NaCl on growth and Cd accumulation of halophyte Spartina alterniflora under CdCl2 stress. South African Journal of Botany, 85: 63–69
Chai M, Shi F, Li R, Qiu G, Liu F, Liu L (2014a). Growth and physiological responses to copper stress in a halophyte Spartina alterniflora (Poaceae). Acta Physiologiae Plantarum, 36(3): 745–754
Chai M, Shi F, Li R, Shen X (2014b). Heavy metal contamination and ecological risk in Spartina alterniflora marsh in intertidal sediments of Bohai Bay, China. Marine Pollution Bulletin, 84(1–2): 115–124
Chai M W, Li R L, Shi F C, Liu F C, Pan X, Cao D, Wen X (2012). Effects of cadmium stress on growth, metal accumulation and organic acids of Spartina alterniflora Loisel. African Journal of Biotechnology, 11(22): 6091–6099
Chi H, Yang L, Yang W, Li Y, Chen Z, Huang L, Chao Y, Qiu R, Wang S (2018). Variation of the bacterial community in the rhizoplane iron plaque of the wetland plant Typha latifolia. International Journal of Environmental Research and Public Health, 15(12): 2610
Coles C A, Rao S R, Yong R N (2000). Lead and cadmium interactions with mackinawite: Retention mechanisms and the role of pH. Environmental Science & Technology, 34(6): 996–1000
Correia R R S, Guimarães J R D (2017). Mercury methylation and sulfate reduction rates in mangrove sediments, Rio de Janeiro, Brazil: The role of different microorganism consortia. Chemosphere, 167: 438–443
Costa-Böddeker S, Thuyên L X, Hoelzmann P, de Stigter H C, van Gaever P, Huy H Đ, Smol J P, Schwalb A (2020). Heavy metal pollution in a reforested mangrove ecosystem (Can Gio Biosphere Reserve, Southern Vietnam): Effects of natural and anthropogenic stressors over a thirty-year history. Science of the Total Environment, 716: 137035
Cundy A, Hopkinson L, Lafite R, Spencer K, Taylor J, Ouddane B, Heppell C, Carey P, Charman R, Shell D, Ullyott S (2005). Heavy metal distribution and accumulation in two Spartina sp.-dominated macrotidal salt marshes from the Seine estuary (France) and the Medway Estuary (UK). Applied Geochemistry, 20(6): 1195–1208
Cutter G A, Velinsky D J (1988). Temporal variations of sedimentary sulfur in a Delaware salt marsh. Marine Chemistry, 23(3–4): 311–327
Dai M, Lu H, Liu W, Jia H, Hong H, Liu J, Yan C (2017). Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation. Ecotoxicology and Environmental Safety, 139: 272–279
de Paula Filho F J, Marins R V, de Lacerda L D, Aguiar J E, Peres T F (2015). Background values for evaluation of heavy metal contamination in sediments in the Parnaíba River Delta Estuary, NE/Brazil. Marine Pollution Bulletin, 91(2): 424–428
de Souza M, Huang C, Chee N, Terry N (1999). Rhizosphere bacteria enhance the accumulation of selenium and mercury in wetland plants. Planta, 209(2): 259–263
Deditius A P, Utsunomiya S, Reich M, Kesler S E, Ewing R C, Hough R, Walshe J (2011). Trace metal nanoparticles in pyrite. Ore Geology Reviews, 42(1): 32–46
Deng J, Guo P, Ji J, Su H, Zhang Y, Wu Y, Sun Y, Wang M (2019). Effects of wetland restoration on sulfur and arylsulfatase in mangrove surface soils at Jinjiang Estuary (Fujian, China). Wetlands, 39(2): 393–402
Dhankher O P, Pilon-Smits E A, Meagher R B, Doty S (2012). Plant biotechnology and agriculture. Biotechnology Education, 3(1): 309–328
Doyle M O, Otte M L (1997). Organism-induced accumulation of iron, zinc and arsenic in wetland soils. Environmental Pollution, 96(1): 1–11
Du W, Tan W, Peralta-Videa J R, Gardea-Torresdey J L, Ji R, Yin Y, Guo H (2017). Interaction of metal oxide nanoparticles with higher terrestrial plants: Physiological and biochemical aspects. Plant Physiology and Biochemistry, 110: 210–225
Du Laing G, Rinklebe J, Vandecasteele B, Meers E, Tack F M (2009). Trace metal behaviour in estuarine and riverine floodplain soils and sediments: A review. Science of the Total Environment, 407(13): 3972–3985
Edwards P J (1998). Sulfur cycling, retention, and mobility in soils: A review. US Department of Agriculture, Forest Service, Northeastern Research Station
Fan J L, Hu Z Y, Ziadi N, Xia X, Wu C Y (2010). Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.). Environmental Pollution, 158(2): 409–415
Fang T, Li X, Zhang G (2005). Acid volatile sulfide and simultaneously extracted metals in the sediment cores of the Pearl River Estuary, South China. Ecotoxicology and Environmental Safety, 61(3): 420–431
Fryzova R, Pohanka M, Martinkova P, Cihlarova H, Brtnicky M, Hladky J, Kynicky J (2018). Reviews of Environmental Contamination and Toxicology Volume 245. de Voogt, P, ed. Cham: Springer International Publishing, 129–156
Gao W, Du Y, Gao S, Ingels J, Wang D (2016). Heavy metal accumulation reflecting natural sedimentary processes and anthropogenic activities in two contrasting coastal wetland ecosystems, eastern China. Journal of Soils and Sediments, 16(3): 1093–1108
Gao X, Song J, Li X, Yuan H, Zhao J, Xing Q, Li P (2020). Sediment quality of the Bohai Sea and the northern Yellow Sea indicated by the results of acid-volatile sulfide and simultaneously extracted metals determinations. Marine Pollution Bulletin, 155: 111147
Ghori N H, Ghori T, Hayat M Q, Imadi S R, Gul A, Altay V, Ozturk M (2019). Heavy metal stress and responses in plants. International Journal of Environmental Science and Technology, 16(3): 1807–1828
González P S, Talano M A, Oller A L W, Ibañez S G, Medina M I, Agostini E (2014). Update on mechanisms involved in arsenic and chromium accumulation, translocation and homeostasis in plants. Heavy Metal Remediation: Transport and Accumulation in Plants. Gupta D K, Chatterjee S, eds. Cham: Springer
Griffin T, Rabenhorst M, Fanning D (1989). Iron and trace metals in some tidal marsh soils of the Chesapeake Bay. Soil Science Society of America Journal, 53(4): 1010–1019
Guo T, Delaune R, Patrick W H (1997). The influence of sediment redox chemistry on chemically active forms of arsenic, cadmium, chromium, and zinc in estuarine sediment. Environment International, 23(3): 305–316
Guo W, Wen Y, Chen Y, Zhou Q (2020). Sulfur cycle as an electron mediator between carbon and nitrate in a constructed wetland microcosm. Frontiers of Environmental Science & Engineering, 14 (4): 57
Haag A F, Kerscher B, Dall’Angelo S, Sani M, Longhi R, Baloban M, Wilson H M, Mergaert P, Zanda M, Ferguson G P (2012). Role of cysteine residues and disulfide bonds in the activity of a legume root nodule-specific, cysteine-rich peptide. Journal of Biological Chemistry, 287(14): 10791–10798
Hancock J T (2019). Hydrogen sulfide and environmental stresses. Environmental and Experimental Botany, 161: 50–56
Hansel C M, Fendorf S, Sutton S, Newville M (2001). Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environmental Science & Technology, 35 (19): 3863–3868
Harbison P (1986). Mangrove muds: A sink and a source for trace metals. Marine Pollution Bulletin, 17(6): 246–250
He H, Li Y, He L F (2018). The central role of hydrogen sulfide in plant responses to toxic metal stress. Ecotoxicology and Environmental Safety, 157: 403–408
He S, Yang X, He Z, Baligar V C (2017). Morphological and physiological responses of plants to cadmium toxicity: A review. Pedosphere, 27(3): 421–438
Hempel M, Botté S E, Negrin V L, Chiarello M N, Marcovecchio J E (2008). The role of the smooth cordgrass Spartina alterniflora and associated sediments in the heavy metal biogeochemical cycle within Bahía Blanca Estuary salt marshes. Journal of Soils and Sediments, 8 (5): 289–297
Hildebrandt U, Regvar M, Bothe H (2007). Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry, 68(1): 139–146
Hu Y, Wu G, Li R, Xiao L, Zhan X (2020). Iron sulphides mediated autotrophic denitrification: An emerging bioprocess for nitrate pollution mitigation and sustainable wastewater treatment. Water Research, 179: 115914
Huang J, Cunningham S (1996). Lead phytoextraction: Species variation in lead uptake and translocation. New Phytologist, 134(1): 75–84
Idaszkin Y L, Carol E S, Barcia-Piedras J M, Bouza P J, Mateos-Naranjo E (2020). Trace metal concentrations in soil-plant complex in rocky shore salt marshes of Central Patagonia. Continental Shelf Research, 211: 104280
Jiang Y, Xi B, Li R, Li M, Xu Z, Yang Y, Gao S (2019). Advances in Fe (III) bioreduction and its application prospect for groundwater remediation: A review. Frontiers of Environmental Science & Engineering, 13(6): 89
Johnston S G, Slavich P, Hirst P (2004). The acid flux dynamics of two artificial drains in acid sulfate soil backswamps on the Clarence River floodplain, Australia. Soil Research (Collingwood, Vic.), 42(6): 623–637
Jørgensen B B (1982). Mineralization of organic matter in the sea bed—the role of sulphate reduction. Nature, 296(5858): 643–645
Joseph P, Nandan S B, Adarsh K, Anu P, Varghese R, Sreelekshmi S, Preethy C, Jayachandran P, Joseph K (2019). Heavy metal contamination in representative surface sediments of mangrove habitats of Cochin, Southern India. Environmental Earth Sciences, 78 (15): 1–11
Karimian N, Johnston S G, Burton E D (2018). Iron and sulfur cycling in acid sulfate soil wetlands under dynamic redox conditions: A review. Chemosphere, 197: 803–816
Kerner M, Wallmann K (1992). Remobilization events involving Cd and Zn from intertidal flat sediments in the Elbe Estuary during the tidal cycle. Estuarine, Coastal and Shelf Science, 35(4): 371–393
Kostka J E, Luther G W III (1995). Seasonal cycling of Fe in saltmarsh sediments. Biogeochemistry, 29(2): 159–181
Kumar S, Prasad S, Yadav K K, Shrivastava M, Gupta N, Nagar S, Bach Q V, Kamyab H, Khan S A, Yadav S, Malav L C (2019). Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches—A review. Environmental Research, 179(PtA): 108792
Kumarathilaka P, Seneweera S, Meharg A, Bundschuh J (2018). Arsenic accumulation in rice (Oryza sativa L.) is influenced by environment and genetic factors. Science of the Total Environment, 642: 485–496
Lacerda L D, Freixo J L, Coelho S M (1997). The effect of Spartina alterniflora Loisel on trace metals accumulation in inter-tidal sediments. Mangroves and Salt Marshes, 1(4): 201–209
Li F, Lin J Q, Liang Y Y, Gan H Y, Zeng X Y, Duan Z P, Liang K, Liu X, Huo Z H, Wu C H (2014). Coastal surface sediment quality assessment in Leizhou Peninsula (South China Sea) based on SEM-AVS analysis. Marine Pollution Bulletin, 84(1–2): 424–436
Li J, Liu J, Lin Y, Yan C, Lu H (2016a). Fraction distribution and migration of heavy metals in mangrove-sediment system under sulphur and phosphorus amendment. Chemistry and Ecology, 32(1): 34–48
Li J, Liu J, Lu H, Jia H, Yu J, Hong H, Yan C (2016b). Influence of the phenols on the biogeochemical behavior of cadmium in the mangrove sediment. Chemosphere, 144: 2206–2213
Li J, Liu J, Yan C, Du D, Lu H (2019a). The alleviation effect of iron on cadmium phytotoxicity in mangrove A. marina. Alleviation effect of iron on cadmium phytotoxicity in mangrove Avicennia marina (Forsk.) Vierh. Chemosphere, 226: 413–420
Li J, Lu H, Liu J, Hong H, Yan C (2015). The influence of flavonoid amendment on the absorption of cadmium in Avicennia marina roots. Ecotoxicology and Environmental Safety, 120: 1–6
Li J, Yu J, Liu J, Yan C, Lu H, Kate L S (2017). The effects of sulfur amendments on the geochemistry of sulfur, phosphorus and iron in the mangrove plant (Kandelia obovata (S. L.)) rhizosphere. Marine Pollution Bulletin, 114(2): 733–741
Li M, Fang A, Yu X, Zhang K, He Z, Wang C, Peng Y, Xiao F, Yang T, Zhang W, Zheng X, Zhong Q, Liu X, Yan Q (2021). Microbially-driven sulfur cycling microbial communities in different mangrove sediments. Chemosphere, 273: 128597
Li R, Morrison L, Collins G, Li A, Zhan X (2016c). Simultaneous nitrate and phosphate removal from wastewater lacking organic matter through microbial oxidation of pyrrhotite coupled to nitrate reduction. Water Research, 96: 32–41
Li Y, Feng W, Chi H, Huang Y, Ruan D, Chao Y, Qiu R, Wang S (2019b). Could the rhizoplane biofilm of wetland plants lead to rhizospheric heavy metal precipitation and iron-sulfur cycle termination? Journal of Soils and Sediments, 19(11): 3760–3772
Lin H, Shi J, Chen X, Yang J, Chen Y, Zhao Y, Hu T (2010). Effects of lead upon the actions of sulfate-reducing bacteria in the rice rhizosphere. Soil Biology & Biochemistry, 42(7): 1038–1044
Lin Y, Fan J, Yu J, Jiang S, Yan C, Liu J (2018). Root activities and arsenic translocation of Avicennia marina (Forsk.) Vierh seedlings influenced by sulfur and iron amendments. Marine Pollution Bulletin, 135: 1174–1182
Liu J, Yan C, Kate L S, Zhang R, Lu H (2010). The distribution of acid-volatile sulfide and simultaneously extracted metals in sediments from a mangrove forest and adjacent mudflat in Zhangjiang Estuary, China. Marine Pollution Bulletin, 60(8): 1209–1216
Liu R, Men C, Liu Y, Yu W, Xu F, Shen Z (2016). Spatial distribution and pollution evaluation of heavy metals in Yangtze estuary sediment. Marine Pollution Bulletin, 110(1): 564–571
Lu H, Yan C, Liu J (2007). Low-molecular-weight organic acids exuded by Mangrove (Kandelia candel (L.) Druce) roots and their effect on cadmium species change in the rhizosphere. Environmental and Experimental Botany, 61(2): 159–166
Luo M, Huang J F, Zhu W F, Tong C (2019). Impacts of increasing salinity and inundation on rates and pathways of organic carbon mineralization in tidal wetlands: A review. Hydrobiologia, 827(1): 31–49
MacFarlane G R, Pulkownik A, Burchett M D (2003). Accumulation and distribution of heavy metals in the grey mangrove, Avicennia marina (Forsk)Vierh: Biological indication potential. Environmental Pollution, 123(1): 139–151
Man K W, Zheng J, Leung A P, Lam P K, Lam M H W, Yen Y F (2004). Distribution and behavior of trace metals in the sediment and porewater of a tropical coastal wetland. Science of the Total Environment, 327(1–3): 295–314
McFarlin C R, Alber M (2013). Foliar DMSO: DMSP ratio and metal content as indicators of stress in Spartina alterniflora. Marine Ecology Progress Series, 474: 1–13
Mostofa M G, Rahman A, Ansary M M U, Watanabe A, Fujita M, Tran L S P (2015). Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Scientific Reports, 5(1): 14078
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa N K (2006). Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Science and Plant Nutrition, 52(4): 464–469
Nedwell D, Embley T, Purdy K (2004). Sulphate reduction, methano-genesis and phylogenetics of the sulphate reducing bacterial communities along an estuarine gradient. Aquatic Microbial Ecology, 37(3): 209–217
Negrin V L, Teixeira B, Godinho R M, Mendes R, Vale C (2017). Phytochelatins and monothiols in salt marsh plants and their relation with metal tolerance. Marine Pollution Bulletin, 121(1–2): 78–84
Neretin L N, Böttcher M E, Jørgensen B B, Volkov I I, Lüschen H, Hilgenfeldt K (2004). Pyritization processes and Greigite formation in the advancing sulfidization front in the upper Pleistocene sediments of the Black Sea. Geochimica et Cosmochimica Acta, 68 (9): 2081–2093
Niazi N K, Burton E D (2016). Arsenic sorption to nanoparticulate mackinawite (FeS): An examination of phosphate competition. Environmental Pollution, 218: 111–117
Nikalje G C, Suprasanna P (2018). Coping with metal toxicity: Cues from halophytes. Frontiers in Plant Science, 9(777): 777
Niu Z S, Pan H, Guo X P, Lu D P, Feng J N, Chen Y R, Tou F Y, Liu M, Yang Y (2018). Sulphate-reducing bacteria (SRB) in the Yangtze Estuary sediments: Abundance, distribution and implications for the bioavailibility of metals. Science of the Total Environment, 634: 296–304
Niu Z S, Yang Y, Tou F Y, Guo X P, Huang R, Xu J, Chen Y R, Hou L J, Liu M, Hochella M F (2020). Sulfate-reducing bacteria (SRB) can enhance the uptake of silver-containing nanoparticles by a wetland plant. Environmental Science. Nano, 7(3): 912–925
Nizoli E C, Luiz-Silva W (2012). Seasonal AVS-SEM relationship in sediments and potential bioavailability of metals in industrialized estuary, southeastern Brazil. Environmental Geochemistry and Health, 34(2): 263–272
O’Geen A T, Budd R, Gan J, Maynard J J, Parikh S J, Dahlgren R A (2010). Advances in Agronomy. Sparks D L, ed.: Academic Press, 1–76
Pallud C, Van Cappellen P (2006). Kinetics of microbial sulfate reduction in estuarine sediments. Geochimica et Cosmochimica Acta, 70(5): 1148–1162
Pardue J H, Patrick W H (2018). Metal contaminated aquatic sediments. Routledge, 169–185
Peralta-Videa J R, Lopez M L, Narayan M, Saupe G, Gardea-Torresdey J (2009). The biochemistry of environmental heavy metal uptake by plants: Implications for the food chain. The International Journal of Biochemistry & Cell Biology, 41(8–9): 1665–1677
Pester M, Knorr K H, Friedrich M W, Wagner M, Loy A (2012). Sulfate-reducing microorganisms in wetlands- fameless actors in carbon cycling and climate change. Frontiers in Microbiology, 3: 72
Pignotti E, Guerra R, Covelli S, Fabbri E, Dinelli E (2018). Sediment quality assessment in a coastal lagoon (Ravenna, NE Italy) based on SEM-AVS and sequential extraction procedure. Science of the Total Environment, 635: 216–227
Rickard D (1995). Kinetics of FeS precipitation: Part 1. Competing reaction mechanisms. Geochimica et Cosmochimica Acta, 59(21): 4367–4379
Rickard D, Morse J W (2005). Acid volatile sulfide (AVS). Marine Chemistry, 97(3–4): 141–197
Rickard D, Mussmann M, Steadman J A (2017). Sedimentary sulfides. Elements, 13(2): 117–122
Rickard D T (1975). Kinetics and mechanism of pyrite formation at low temperatures. American Journal of Science, 275(6): 636–652
Romero L C, Aroca M Á, Laureano-Marín A M, Moreno I, García I, Gotor C (2014). Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Molecular Plant, 7(2): 264–276
Rousseau H, Rousseau-Gueutin M, Dauvergne X, Boutte J, Simon G, Marnet N, Bouchereau A, Guiheneuf S, Bazureau J P, Morice J, Ravanel S, Cabello-Hurtado F, Ainouche A, Salmon A, Wendel J F, Ainouche M L (2017). Evolution of DMSP (dimethylsulfoniopropionate) biosynthesis pathway: Origin and phylogenetic distribution in polyploid Spartina (Poaceae, Chloridoideae). Molecular Phylogenetics and Evolution, 114: 401–414
Roychoudhury A N, Cowan D, Porter D, Valverde A (2013). Dissimilatory sulphate reduction in hypersaline coastal pans: an integrated microbiological and geochemical study. Geobiology, 11 (3): 224–233
SEPA (2002). Marine Sediment Quality (GB 18668-2002). Beijing: Standards Press of China
Shi C, Ding H, Zan Q, Li R (2019). Spatial variation and ecological risk assessment of heavy metals in mangrove sediments across China. Marine Pollution Bulletin, 143: 115–124
Shyleshchandran M N, Mohan M, Ramasamy E V (2018). Risk assessment of heavy metals in Vembanad Lake sediments (southwest coast of India), based on acid-volatile sulfide (AVS)-simultaneously extracted metal (SEM) approach. Environmental Science and Pollution Research International, 25(8): 7333–7345
Singh V P, Singh S, Kumar J, Prasad S M (2015). Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: Possible involvement of nitric oxide. Journal of Plant Physiology, 181: 20–29
Singleton R (1993). The Sulfate-Reducing Bacteria: Contemporary Perspectives. New York: Springer, 1–20
Spencer K L (2002). Spatial variability of metals in the inter-tidal sediments of the Medway Estuary, Kent, UK. Marine Pollution Bulletin, 44(9): 933–944
Stewart P S, Franklin M J (2008). Physiological heterogeneity in biofilms. Nature Reviews. Microbiology, 6(3): 199–210
Sun Z, Li J, He T, Ren P, Zhu H, Gao H, Tian L, Hu X (2017). Spatial variation and toxicity assessment for heavy metals in sediments of intertidal zone in a typical subtropical estuary (Min River) of China. Environmental Science and Pollution Research International, 24(29): 23080–23095
Sun Z, Mou X, Tong C, Wang C, Xie Z, Song H, Sun W, Lv Y (2015). Spatial variations and bioaccumulation of heavy metals in intertidal zone of the Yellow River Estuary, China. Catena, 126: 43–52
Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011). Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annual Review of Plant Biology, 62(1): 157–184
Thomas F, Giblin A E, Cardon Z G, Sievert S M (2014). Rhizosphere heterogeneity shapes abundance and activity of sulfur-oxidizing bacteria in vegetated salt marsh sediments. Frontiers in Microbiology, 5: 309
Tourova T P, Kovaleva O L, Sorokin D Y, Muyzer G (2010). Ribulose-1,5-bisphosphate carboxylase/oxygenase genes as a functional marker for chemolithoautotrophic halophilic sulfur-oxidizing bacteria in hypersaline habitats. Microbiology, 156(7): 2016–2025
Tripathi R D, Srivastava S, Mishra S, Singh N, Tuli R, Gupta D K, Maathuis F J (2007). Arsenic hazards: strategies for tolerance and remediation by plants. Trends in Biotechnology, 25(4): 158–165
Viehweger K (2014). How plants cope with heavy metals. Botanical Studies, 55(1): 35
Wang C, Lin D, Wang P, Ao Y, Hou J, Zhu H (2015a). Seasonal and spatial variations of acid-volatile sulphide and simultaneously extracted metals in the Yangtze River Estuary. Chemistry and Ecology, 31(5): 466–477
Wang P, Menzies N W, Lombi E, Sekine R, Blamey F P C, Hernandez-Soriano M C, Cheng M, Kappen P, Peijnenburg W J, Tang C, Kopittke P M (2015b). Silver sulfide nanoparticles (Ag2S-NPs) are taken up by plants and are phytotoxic. Nanotoxicology, 9(8): 1041–1049
Wang Y, Zhou L, Zheng X, Qian P, Wu Y (2013). Influence of Spartina alterniflora on the mobility of heavy metals in salt marsh sediments of the Yangtze River Estuary, China. Environmental Science and Pollution Research International, 20(3): 1675–1685
Weng B, Xie X, Weiss D J, Liu J, Lu H, Yan C (2012). Kandelia obovata (S. L.) Yong tolerance mechanisms to Cadmium: Subcellular distribution, chemical forms and thiol pools. Marine Pollution Bulletin, 64(11): 2453–2460
Wilkin R T, Beak D G (2017). Uptake of nickel by synthetic mackinawite. Chemical Geology, 462: 15–29
Wilson L G, Bressan R A, Filner P (1978). Light-dependent emission of hydrogen sulfide from plants. Plant Physiology, 61(2): 184–189
Wright D J, Otte M L (1999). Wetland plant effects on the biogeochemistry of metals beyond the rhizosphere. JSTOR, 3–10
Wu Q, Ma Q, Wang J, Jiang Z, Wang X L (2007). The AVS in surface sediment of near sea area of Huanghe Estuary. Marine Environmental Science, 26(2): 126–129 (in Chinese)
Wu S, Li R, Xie S, Shi C (2019). Depth-related change of sulfate-reducing bacteria community in mangrove sediments: The influence of heavy metal contamination. Marine Pollution Bulletin, 140: 443–450
Wu Y, Leng Z, Li J, Jia H, Yan C, Hong H, Wang Q, Lu Y, Du D (2022). Increased fluctuation of sulfur alleviates cadmium toxicity and exacerbates the expansion of Spartina alterniflora in coastal wetlands. Environmental Pollution, 292(Pt B): 118399
Wu Z, Naveed S, Zhang C, Ge Y (2020). Adequate supply of sulfur simultaneously enhances iron uptake and reduces cadmium accumulation in rice grown in hydroponic culture. Environmental Pollution, 262: 114327
Xia L, Yang W, Zhao H, Xiao Y, Qing H, Zhou C, An S (2015). High soil sulfur promotes invasion of exotic Spartina alterniflora into native Phragmites australis marsh. Clean (Weinheim), 43(12): 1666–1671
Xie X, Weiss D J, Weng B, Liu J, Lu H, Yan C (2013). The short-term effect of cadmium on low molecular weight organic acid and amino acid exudation from mangrove (Kandelia obovata (S. L.) Yong) roots. Environmental Science and Pollution Research International, 20(2): 997–1008
Yadav S (2010). Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African Journal of Botany, 76(2): 167–179
Yamaguchi N, Ohkura T, Takahashi Y, Maejima Y, Arao T (2014). Arsenic distribution and speciation near rice roots influenced by iron plaques and redox conditions of the soil matrix. Environmental Science & Technology, 48(3): 1549–1556
Yamauchi T, Fukazawa A, Nakazono M (2017). METALLOTHIONEIN genes encoding ROS scavenging enzymes are down-regulated in the root cortex during inducible aerenchyma formation in rice. Plant Signaling & Behavior, 12(11): e1388976
Yang J, Ma Z, Ye Z, Guo X, Qiu R (2010). Heavy metal (Pb, Zn) uptake and chemical changes in rhizosphere soils of four wetland plants with different radial oxygen loss. Journal of Environmental Sciences (China), 22(5): 696–702
Yang J, Ye Z (2009). Metal accumulation and tolerance in wetland plants. Frontiers of Biology in China, 4(3): 282–288
Yang X, He Q, Guo F, Liu X, Chen Y (2021). Translocation and biotoxicity of metal (oxide) nanoparticles in the wetland-plant system. Frontiers of Environmental Science & Engineering, 15(6): 138
Yang Y, Chen T, Sumona M, Gupta B S, Sun Y, Hu Z, Zhan X (2017). Utilization of iron sulfides for wastewater treatment: A critical review. Reviews in Environmental Science and Biotechnology, 16 (2): 289–308
Youli Z, Jian L, Zhanrui L, Daolin D (2020). The influence of root exudate flavonoids on sulfur species distribution in mangrove sediments polluted with cadmium. Wetlands, 40(6): 2671–2678
Younis A M, El-Zokm G M, Okbah M A (2014). Spatial variation of acid-volatile sulfide and simultaneously extracted metals in Egyptian Mediterranean Sea lagoon sediments. Environmental Monitoring and Assessment, 186(6): 3567–3579
Youssef T, Saenger P (1998). Photosynthetic gas exchange and accumulation of phytotoxins in mangrove seedlings in response to soil physico-chemical characteristics associated with waterlogging. Tree Physiology, 18(5): 317–324
Yu Q, Si G, Zong T, Mulder J, Duan L (2019). High hydrogen sulfide emissions from subtropical forest soils based on field measurements in south China. Science of the Total Environment, 651(Pt 1): 1302–1309
Yu X Z, Lu M R, Zhang X H (2017). The role of iron plaque in transport and distribution of chromium by rice seedlings. Cereal Research Communications, 45(4): 598–609
Zandi P, Yang J, Xia X, Tian Y, Li Q, Możdżeń K, Barabasz-Krasny B, Wang Y (2020). Do sulfur addition and rhizoplane iron plaque affect chromium uptake by rice (Oryza sativa L.) seedlings in solution culture? Journal of Hazardous Materials, 388: 121803
Zecchin S, Colombo M, Cavalca L (2019). Exposure to different arsenic species drives the establishment of iron- and sulfur-oxidizing bacteria on rice root iron plaques. World Journal of Microbiology & Biotechnology, 35(8): 117
Zeleke J, Sheng Q, Wang J G, Huang M Y, Xia F, Wu J H, Quan Z X (2013). Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Frontiers in Microbiology, 4: 243
Zhang C, Yu Z G, Zeng G M, Jiang M, Yang Z Z, Cui F, Zhu M Y, Shen L Q, Hu L (2014). Effects of sediment geochemical properties on heavy metal bioavailability. Environment International, 73: 270–281
Zhang H, Cui B, Xiao R, Zhao H (2010). Heavy metals in water, soils and plants in riparian wetlands in the Pearl River Estuary, South China. Procedia Environmental Sciences, 2(5): 1344–1354
Zhang L, Ni Z, Wu Y, Zhao C, Liu S, Huang X (2020). Concentrations of porewater heavy metals, their benthic fluxes and the potential ecological risks in Daya Bay, South China. Marine Pollution Bulletin, 150: 110808
Zhang L, Ye X, Feng H, Jing Y, Ouyang T, Yu X, Liang R, Gao C, Chen W (2007). Heavy metal contamination in western Xiamen Bay sediments and its vicinity, China. Marine Pollution Bulletin, 54(7): 974–982
Zhang M, He P, Qiao G, Huang J, Yuan X, Li Q (2019a). Heavy metal contamination assessment of surface sediments of the Subei Shoal, China: Spatial distribution, source apportionment and ecological risk. Chemosphere, 223: 211–222
Zhang Q, Yan Z, Li X (2021). Iron plaque formation and rhizosphere iron bacteria in Spartina alterniflora and Phragmites australis on the redoxcline of tidal flat in the Yangtze River Estuary. Geoderma, 392: 115000
Zhang Y, Wei D, Morrison L, Ge Z, Zhan X, Li R (2019b). Nutrient removal through pyrrhotite autotrophic denitrification: Implications for eutrophication control. Science of the Total Environment, 662: 287–296
Zheng Y, Bu N S, Long X E, Sun J, He C Q, Liu X Y, Cui J, Liu D X, Chen X P (2017). Sulfate reducer and sulfur oxidizer respond differentially to the invasion of Spartina alterniflora in estuarine salt marsh of China. Ecological Engineering, 99: 182–190
Zhou Y W, Peng Y S, Li X L, Chen G Z (2011). Accumulation and partitioning of heavy metals in mangrove rhizosphere sediments. Environmental Earth Sciences, 64(3): 799–807
Zou R, Wang L, Li Y C, Tong Z, Huo W, Chi K, Fan H (2020). Cadmium absorption and translocation of amaranth (Amaranthus mangostanus L.) affected by iron deficiency. Environmental Pollution, 256: 113410
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant Nos. 32071521, 31800429, and 42067012), the Natural Science Foundation of Jiangsu Province (Nos. BK20170540 and BK20210751), the Scientific Research Foundation for Senior Talent of Jiangsu University, China (No. 20JDG067), the Science and Technology Program of Gansu Province of China (No. 20JR5RA532), the MEL Visiting Fellowship of Xiamen University and Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment, China. The authors would like to thank Dr. Shili Miao from South Florida Water Management District and Xuexue Yang for their effort in manuscript improvement. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Highlights
• In sediments, the transformation of sulfides may lead to the release of heavy metals.
• In the rhizosphere, sulfur regulates the uptake of heavy metals by plants.
• In plants, sulfur mediates a series of heavy metal tolerance mechanisms.
• Explore interactions between sulfur and heavy metals on different scales is needed.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Wu, Y., Leng, Z., Li, J. et al. Sulfur mediated heavy metal biogeochemical cycles in coastal wetlands: From sediments, rhizosphere to vegetation. Front. Environ. Sci. Eng. 16, 102 (2022). https://doi.org/10.1007/s11783-022-1523-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11783-022-1523-x