Abstract
The biogeochemistry of dissolved selenium (Se) was investigated over 3 years (2015–2017) in the subtropical, warm monomictic and meso-eutrophic Lake Kinneret (Sea of Galilee, Israel). We monitored seasonal variation and vertical distribution of dissolved total Se (T.Se), inorganic oxyanions (Se(IV) & Se(VI)), reduced Se fraction (Red.Se), organic (Org.Se) and volatile Se compounds. T.Se varied between ~ 100 and 160 ng L−1 with Red.Se comprising 40–80% of the Se inventory, and Se(VI) dominating over Se(IV) most of the time. The variation in T.Se and species correlated with winter holomixis vs. summer fall stratification periods. The annual cycle includes: (a) increase of T.Se from fall/winter to spring, representing increased allochthonous Se input flux, along with Se recycling via holomixis; (b) decrease of T.Se from spring to the end of the year, representing the diminishing Se inputs and the evolving output fluxes to the lake’s bottom and to the atmosphere. Org.Se variations are directly associated with Chlorophyll-a and primary production attesting for the significant role of phytoplankton activity in the Se cycle. An important Se output flux comprises spring to summer Se uptake by phytoplankton and further volatile compounds production and volatilization accounting for ~ 10% of estimated Se input. The similarity of total dissolved Se concentrations in this work and from mid 1990s attests for long-term stability of the Se inventory. The TVSe concentrations in lacustrine systems being similar to that of estuary systems, the biological role of phytoplankton and eventually the degradation of organic material may produce similar fluxes of volatile Se to the atmosphere.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10533-021-00877-6/MediaObjects/10533_2021_877_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10533-021-00877-6/MediaObjects/10533_2021_877_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10533-021-00877-6/MediaObjects/10533_2021_877_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10533-021-00877-6/MediaObjects/10533_2021_877_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10533-021-00877-6/MediaObjects/10533_2021_877_Fig5_HTML.png)
Similar content being viewed by others
Data availability
Data collected and used in this manuscript are available in supplementary information file.
Code availability
Not applicable.
References
Amouroux D, Donard OFX (1996) Maritime emission of selenium to the atmosphere in Eastern Mediterranean seas. Geophys Res Lett 23:1777–1780. https://doi.org/10.1029/96GL01271
Amouroux D, Donard OFX (1997) Evasion of selenium to the atmosphere via biomethylation processes in the Gironde estuary, France. Mar Chem 58:173–188. https://doi.org/10.1016/S0304-4203(97)00033-9
Amouroux D, Pécheyran C, Donard OFX (2000) Formation of volatile selenium species in synthetic seawater under light and dark experimental conditions. Appl Organomet Chem 14:236–244. https://doi.org/10.1002/(SICI)1099-0739(200005)14:5%3C236::AID-AOC982%3E3.0.CO;2-U
Amouroux D, Liss PS, Tessier E, Hamren-Larsson M, Donard OFX (2001) Role of ocens as biogenic sources of selenium. Earth Planet Sci Lett 189:277–283. https://doi.org/10.1016/S0012-821X(01)00370-3
Balistrieri LS, Chao TT (1987) Selenium adsorption by goethite. Soil Sci Soc Am J 51:1145–1151. https://doi.org/10.2136/sssaj1987.03615995005100050009x
Bender J, Gould JP, Vatcharapijarn Y, Saha G (1991) Uptake, transformation and fixation of Se (VI) by a mixed selenium-tolerant ecosystem. Water Air Soil Pollut 59:359–367. https://doi.org/10.1007/BF00211843
Berman T, Zohary T, Nishri A, Sukenik A (2014) General background. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret: ecology and management. Springer, Heidelberg, pp 1–15. https://doi.org/10.1007/978-94-017-8944-8
Buchs B, Evangelou MWH, Winkel LHE, Lenz M (2013) Colloidal properties of nanoparticular biogenic selenium govern environmental fate and bioremediation effectiveness. Environ Sci Technol 47:2401–2407. https://doi.org/10.1021/es304940s
Chau YK, Wong PTS, Silverberg BA, Luxon PL, Bengert GA (1976) Methylation of selenium in the aquatic environment. Science 192:1130–1131. https://doi.org/10.1126/science.192.4244.1130
Chasteen TG, Bentley R (2003) Biomethylation of selenium and tellurium: microorganisms and plants. Chem Rev 103:1–25. https://doi.org/10.1021/cr010210
Chouhan R, Banerjee M (2010) Two cyanobacteria Hapalosiphon sp. and Gloeocapsa sp. in amelioration of selenium toxicity. J Appl Biosci 36:137–140
Cole JJ, Caraco NF (1998) Atmospheric exchange of carbon dioxide in a low-wind oligotrophic lake measured by the addition of SF6. Limnol Oceanogr 43:647–656. https://doi.org/10.4319/lo.1998.43.4.0647
Conde JE, Sanz Alaejos M (1997) Selenium concentrations in natural and environmental waters. Chem Rev 97:1979–2004. https://doi.org/10.1021/cr960100g
Cooke TD, Bruland KW (1987) Aquatic chemistry of selenium: evidence of biomethylation. Environ Sci Technol 21:1214–1219. https://doi.org/10.1021/es00165a009
Cutter GA (1978) Species determination of selenium in natural waters. Anal Chim Acta 98:59–66. https://doi.org/10.1016/S0003-2670(01)83238-4
Cutter GA, Bruland KW (1984) The marine biogeochemistry of selenium: a re-evaluation. Limnol Oceanogr 29:1179–1192. https://doi.org/10.4319/lo.1984.29.6.1179
Darrouzès J, Bueno M, Simon S, Pannier F, Potin-Gautier M (2008) Advantages of hydride generation interface for selenium speciation in waters by high performance liquid chromatography-inductively coupled plasma mass spectrometry coupling. Talanta 75:362–368. https://doi.org/10.1016/j.talanta.2007.11.020
Dauthieu M, Bueno M, Darrouzes J, Gilon N, Potin-Gautier M (2006) Evaluation of porous graphitic carbon stationary phase for simultaneous preconcentration and separation of organic and inorganic selenium species in “clean” water systems. J Chromatogr A 1114:34–39. https://doi.org/10.1016/j.chroma.2006.02.018
Diaz X, Johnson WP, Oliver WA, Naftz DL (2009) Volatile selenium flux from the great Salt Lake, Utah. Environ Sci Technol 43:53–59. https://doi.org/10.1021/es801638w
Domagalski JL, Orem WH, Eugster HP (1989) Organic geochemistry and brine composition in Great Salt, Mono, and Walker Lakes. Geochim Cosmochim Acta 53:2857–2872. https://doi.org/10.1016/0016-7037(89)90163-4
Duan L, Song J, Li X, Yuan H, Xu S (2010) Distribution of selenium and its relationship to the eco-environment in Bohai Bay seawater. Mar Chem 121:87–99. https://doi.org/10.1016/j.marchem.2010.03.007
Eckert W, Conrad R (2007) Sulfide and methane evolution in the hypolimnion of a subtropical lake: a three-year study. Biogeochemistry 82:67–76. https://doi.org/10.1007/s10533-006-9053-3
Fan TW-M, Higashi RM, Lane AN (1998) Biotransformations of selenium oxyanion by filamentous cyanophyte-dominated mat cultured from agricultural drainage waters. Environ Sci Technol 32:3185–3193. https://doi.org/10.1021/es9708833
Fernández-Martínez A, Charlet L (2009) Selenium environmental cycling and bioavailability: a structural chemist point of view. Rev Environ Sci Biotechnol 8:81–110. https://doi.org/10.1007/s11157-009-9145-3
Ginzburg B, Chalifa I, Gun J, Dor I, Hadas O, Lev O (1998) DMS formation by dimethylsulfoniopropionate route in freshwater. Environ Sci Technol 32:2130–2136. https://doi.org/10.1021/es9709076
Ginzburg B, Dor I, Chalifa I, Hadas O, Lev O (1999) Formation of dimethyloligosulfides in Lake Kinneret: biogenic formation of inorganic oligosulfide intermediates under oxic conditions. Environ Sci Technol 33:571–579. https://doi.org/10.1021/es980636e
Guo L, Frankenberger WT, Jury WA (1999) Evaluation of simultaneous reduction and transport of selenium in saturated soil columns. Water Resour Res 35:663–669. https://doi.org/10.1029/1998WR900074
Hadas O (2014) Microbial processes within the nitrogen cycle. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret: Ecology and Management. Springer, Heidelberg, pp 381–396. https://doi.org/10.1007/978-94-017-8944-8
Hadas O, Pinkas R (1995) Sulphate reduction in the hypolimnion and sediments of Lake Kinneret, Israel. Freshw Biol 33:63–72. https://doi.org/10.1111/j.1365-2427.1995.tb00386.x
Hambright KD, Zohary T (1998) Lakes Hula and Agmon: destruction and creation of wetland ecosystems in northern Israel. Wetl Ecol Manag 6:83–89. https://doi.org/10.1023/A:1008441015990
Harrison PJ, Yu PW, Thompson PA, Price NM, Phillips DJ (1988) Survey of selenium requirements in marine phytoplankton. Mar Ecol Prog Ser 47:89–96
Hu M, Yang Y, Martin J-M, Yin K, Harrison PJ (1997) Preferential uptake of Se(IV) over Se(VI) and the production of dissolved organic Se by marine phytoplankton. Mar Environ Res 44:225–231. https://doi.org/10.1016/S0141-1136(97)00005-6
Hu H, Mylon SE, Benoit G (2007) Volatile organic sulfur compounds in a stratified lake. Chemosphere 67:911–919. https://doi.org/10.1016/j.chemosphere.2006.11.012
Ivanenko NV (2018) The role of microorganisms in transformation of selenium in marine waters. Russ J Mar Biol 44:87–93. https://doi.org/10.1134/S1063074018020049
Knossow N, Blonder B, Eckert W, Turchyn AV, Antler G, Kamyshny A (2015) Annual sulfur cycle in a warm monomictic lake with sub-millimolar sulfate concentrations. Geochem Trans 16:7. https://doi.org/10.1186/s12932-015-0021-5
Lanceleur L, Tessier E, Pienitz R, Cloquet C, Amouroux D (2019) Cycling and atmospheric exchanges of selenium in Canadian subarctic thermokarst ponds. Biogeochemistry 145:193–211. https://doi.org/10.1007/s10533-019-00599-w
Lindström K (1983) Selenium as a growth factor for plankton algae in laboratory experiments and in some Swedish lakes. In: Forsberg C, Johansson J-Å (eds) Hydrobiologia, vol 101. Springer, New York, pp 35–47. https://doi.org/10.1007/BF00008655
Lenz M, Lens PNL (2009) The essential toxin: the changing perception of selenium in environmental sciences. Sci Tot Environ 407:3620–3633. https://doi.org/10.1016/j.scitotenv.2008.07.056
Luxem KE, Vriens B, Behra R, Winkel LHE (2017) Studying selenium and sulfur volatilisation by marine algae Emiliania huxleyi and Thalassiosira oceanica in culture. Environ Chem 14:199–206. https://doi.org/10.1071/EN16184
Mason RP, Soerensen AL, Dimento BP, Balcom PH (2018) The global marine selenium cycle: insights from measurements and modeling. Global Biogeochem Cycles 32:1720–1737. https://doi.org/10.1029/2018GB006029
McNeal JM, Balistrieri LS (1989) Geochemistry and occurrence of selenium: an overview. In: Jacobs LW (ed) Selenium in agriculture and the environment. American Society of Agronomy, Madison, pp 1–13. https://doi.org/10.2136/sssaspecpub23.c1
Measures CI, Burton JD (1980) The vertical distribution and oxidation states of dissolved selenium in the Atlantic. Earth Planet Sci Lett 46:385–396. https://doi.org/10.1016/0012-821X(80)90052-7
Mehdi Y, Hornick J-L, Istasse L, Dufrasne I (2013) Selenium in the environment, metabolism and involvement in body functions. Molecules 18:3292–3311. https://doi.org/10.3390/molecules18033292
Mortimer CH (1981) The oxygen content of air-saturated fresh waters over ranges of temperature and atmospheric pressure of limnological interest. SIL Commun 1953–1996(22):1–23. https://doi.org/10.1080/05384680.1981.11904000
Nakaguchi Y, Hiraki K (1993) Selenium (IV), selenium (VI) and organic selenium in Lake Biwa, the Yodo River and Osaka Bay. Geochem J 27:367–374. https://doi.org/10.2343/geochemj.27.367
Nakamaru YM, Altansuvd J (2014) Speciation and bioavailability of selenium and antimony in non-flooded and wetland soils: a review. Chemosphere 111:366–371. https://doi.org/10.1016/j.chemosphere.2014.04.024
Nancharaiah YV, Lens PNL (2015) Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol Rev 79:61–80. https://doi.org/10.1128/MMBR.00037-14
Neumann PM, De Souza MP, Pickering IJ, Terry N (2003) Rapid microalgal metabolism of selenate to volatile dimethylselenide. Plant Cell Environ 26:897–905. https://doi.org/10.1046/j.1365-3040.2003.01022.x
Niedzielski P, Siepak M, Grabowski K (2002) Microtrace contents of arsenic, antimony and selenium in surface waters of Pszczewski landscape park as a region potentially free from anthropogenic pressure. Pol J Environ Stud 11:547–553
Nishri A, Brenner IB, Hall GEM, Taylor HE (1999) Temporal variations in dissolved selenium in Lake Kinneret (Israel). Aquat Sci 61:215–233. https://doi.org/10.1007/s000270050063
Oremland RS, Hollibaugh JT, Maest AS, Presser TS, Miller LG, Charles W, Maest ANNS (1989) Selenate reduction to elemental selenium by anaerobic bacteria in sediments and culture. Appl Environ Microbiol 55:2333–2343
Ostrovsky I, Rimmer A, Yacobi YZ, Nishri A, Sukenik A, Hadas O, Zohary T (2013) Long-term changes in the Lake Kinneret ecosystem: the effects of climate change and anthropogenic factors. In: Goldman CR, Kumagai M, Robarts RD (eds) Climate change and global warming of inland waters: impacts and mitigation for ecosystems and societies. Wiley, New York, pp 271–293. https://doi.org/10.1002/9781118470596.ch16
Pilon-Smits EAH, Quinn CF (2010) Selenium metabolism in plants. In: Hell R, Mendel RR (eds) Cell biology of metals and nutrients. Springer, New York, pp 225–241. https://doi.org/10.1007/978-3-642-10613-2_10
Pokrovsky OS, Bueno M, Manasypov RM, Shirokova LS, Karlsson J, Amouroux D (2018) Dissolved organic matter controls on seasonal and spatial selenium concentration variability in thaw lakes across a permafrost gradient. Environ Sci Technol 52:10254–10262. https://doi.org/10.1021/acs.est.8b00918
Ponton DE, Hare L (2013) Relating selenium concentrations in a planktivore to selenium speciation in lakewater. Environ Pollut 176:254–260. https://doi.org/10.1016/j.envpol.2013.01.032
Ponton DE, Fortin C, Hare L (2018) Organic selenium, selenate, and selenite accumulation by lake plankton and the alga Chlamydomonas reinhardtii at different pH and sulfate concentrations. Environ Toxicol Chem 37:2112–2122. https://doi.org/10.1002/etc.4158
Rimmer A, Gal G (2003) Estimating the saline springs component in the solute and water balance of Lake Kinneret, Israel. J Hydrol 284:228–243. https://doi.org/10.1016/j.jhydrol.2003.08.006
Rimmer A, Givati A (2014) Hydrology. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret: ecology and management. Springer, Heidelberg, pp 97–112. https://doi.org/10.1007/978-94-017-8944-8
Robberecht H, Van Grieken R, Van Sprundel M, Vanden Berghe D, Deelstra H (1983) Selenium in environmental and drinking waters of Belgium. Sci Tot Environ 26:163–172. https://doi.org/10.1016/0048-9697(83)90109-2
Rom M, Berger D, Teltsch B, Markel D (2014) Material loads from the Jordan River. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret: ecology and management. Springer, Heidelberg, pp 309–328. https://doi.org/10.1007/978-94-017-8944-8
Sela-Adler M, Said-Ahmad W, Sivan O, Eckert W, Kiene RP, Amrani A (2016) Isotopic evidence for the origin of dimethylsulfide and dimethylsulfoniopropionate-like compounds in a warm, monomictic freshwater lake. Environ Chem 13:340–351. https://doi.org/10.1071/EN15042
Shaked Y, Erel Y, Sukenik A (2004) The biogeochemical cycle of iron and associated elements in Lake Kinneret. Geochim Cosmochim Acta 68:1439–1451. https://doi.org/10.1016/j.gca.2003.09.018
Simmons DBD, Wallschläger D (2011) Release of reduced inorganic selenium species into waters by the green fresh water algae chlorella vulgaris. Environ Sci Technol 45:2165–2171. https://doi.org/10.1021/es103337p
Sukenik A, Zohary T, Markel D (2014) The monitoring program. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret: ecology and management. Springer, Heidelberg, pp 561–576. https://doi.org/10.1007/978-94-017-8944-8
Tanzer D, Heumann KG (1991) Determination of dissolved selenium species in environmental water samples using isotope dilution mass spectrometry. Anal Chem 63:1984–1989. https://doi.org/10.1021/ac00018a016
Tessier E, Amouroux D, Abril G, Lemaire E, Donard OFX (2002a) Formation and volatilisation of alkyl-iodides and -selenides in macrotidal estuaries. Biogeochemistry 59:183–206. https://doi.org/10.1023/A:1015550931365
Tessier E, Amouroux D, Donard OFX (2002) Biogenic volatilization of trace elements from European estuaries. In: Cai Y, Braids OC (eds) Biogeochemistry of environmentally important trace elements. ACS Symposium Series, vol 835, pp 151–165. https://doi.org/10.1021/bk-2003-0835.ch012
Velinsky DJ, Cutter GA (1990) Determination of elemental selenium and pyrite-selenium in sediments. Anal Chim Acta 235:419–425. https://doi.org/10.1016/S0003-2670(00)82102-9
Vriens B, Behra R, Voegelin A, Zupanic A, Winkel LHE (2016) Selenium uptake and methylation by the Microalga Chlamydomonas reinhardtii. Environ Sci Technol 50:711–720. https://doi.org/10.1021/acs.est.5b04169
Vriens B, Ammann AA, Hagendorfer H, Lenz M, Berg M, Winkel LHE (2014) Quantification of methylated selenium, sulfur, and arsenic in the environment. PLoS ONE 9(7):e102906. https://doi.org/10.1371/journal.pone.0102906
Wang D, Alfthan G, Aro A, Lahermo P, Väänänen P (1994) The impact of selenium fertilisation on the distribution of selenium in rivers in Finland. Agric Ecosyst Environ 50:133–149. https://doi.org/10.1016/0167-8809(94)90132-5
Wang D, Alfthan G, Aro A, Mäkelä A, Knuuttila S, Hammar T (1995) The impact of selenium supplemented fertilization on selenium in lake ecosystems in Finland. Agric Ecosyst Environ 54:137–148. https://doi.org/10.1016/0167-8809(94)00574-X
Wen H, Carignan J (2007) Reviews on atmospheric selenium: emissions, speciation and fate. Atmos Environ 41:7151–7165. https://doi.org/10.1016/j.atmosenv.2007.07.035
Weres O, Jaouni A-R, Tsao L (1989) The distribution, speciation and geochemical cycling of selenium in a sedimentary environment, Keterston Reservoir, California USA. Appl Geochem 4:543–563. https://doi.org/10.1016/0883-2927(89)90066-8
Weres O, Bowman HR, Goldstein A, Smith EC, Tsao L, Harnden W (1990) The effect of nitrate and organic matter upon mobility of selenium in groundwater and in a water treatment process. Water Air Soil Pollut 49:251–272. https://doi.org/10.1007/BF00507068
Winkel LHE, Johnson CA, Lenz M, Grundl T, Leupin OX, Amini M, Charlet L (2012) Environmental selenium research: from microscopic processes to global understanding. Environ Sci Technol 46:571–579. https://doi.org/10.1021/es203434d
Winkel LHE, Vriens B, Jones GD, Schneider LS, Pilon-Smits E, Bañuelos GS (2015) Selenium cycling across soil-plant-atmosphere interfaces: a critical review. Nutrients 7:4199–4239. https://doi.org/10.3390/nu7064199
Wrench JJ, Measures CI (1982) Temporal variations in dissolved selenium in a coastal ecosystem. Nature 299:431–433. https://doi.org/10.1038/299431a0
Zhang Y, Zahir ZA, Frankenberger WT (2004) Fate of colloidal-particulate elemental selenium in aquatic systems. J Environ Qual 33:559–564. https://doi.org/10.2134/jeq2004.5590
Zohary T (2004) Changes to the phytoplankton assemblage of Lake Kinneret after decades of a predictable, repetitive pattern. Freshw Biol 49:1355–1371. https://doi.org/10.1111/j.1365-2427.2004.01271.x
Zohary T, Sukenik A, Berman T, Nishri A (eds) (2014a) Lake Kinneret: ecology and management. Springer, Heidelberg, p 683. https://doi.org/10.1007/978-94-017-8944-8
Zohary T, Yacobi YZ, Alster A, Fishbein T, Lippman S, Tibor G (2014b) Phytoplankton. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret: ecology and management. Springer, Heidelberg, pp 161–190. https://doi.org/10.1007/978-94-017-8944-8
Acknowledgements
Y. Be’eri-Shlevin wishes to dedicate this paper to D. Solnik.
Funding
The research leading to these results received funding from the Israeli Water Authority (grant #4500963096) and, Aquitaine Region (AQUITRACES Project n° 20131206001–13010973) & ANR IA RSNR (AMORAD project n°ANR-11-RSNR-0002) for equipment funding. The financial support of A. Romero—Rama Doctoral fellowship was received from UPPA and IPREM.
Author information
Authors and Affiliations
Contributions
YB-S: Conceptualization, Investigation, Resources, Writing-original draft, Writing-review & editing, Funding acquisition. MB: Conceptualization, Investigation, Validation, Writing-original draft, Writing-review & editing, Funding acquisition. ET: Conceptualization, Investigation, Validation, Writing-review & editing. AR-R: Conceptualization, Formal analysis, Writing-original draft. AS: Conceptualization, Investigation, Resources, Writing-review & editing, Funding acquisition. TZ: Conceptualization, Resources, Writing-original draft, Writing-review & editing, Funding acquisition. DA: Conceptualization, Writing-original draft, Writing-review & editing, Funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict or competing interest to declare.
Additional information
Responsible Editor: R. Kelman Wieder.
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.
Rights and permissions
About this article
Cite this article
Be’eri-Shlevin, Y., Bueno, M., Tessier, E. et al. Biogeochemistry of selenium compounds in the water column of warm monomictic Lake Kinneret. Biogeochemistry 157, 291–311 (2022). https://doi.org/10.1007/s10533-021-00877-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-021-00877-6