Research article

Uptake and reduction of Se(IV) in two heterotrophic aerobic Pseudomonads strains isolated from boreal bog environment

  • Received: 16 August 2017 Accepted: 28 September 2017 Published: 10 October 2017
  • Selenite (Se(IV), SeO32−) uptake and the effect of selenite supplement on protein synthesis was investigated in two Pseudomonas sp. strains isolated from a boreal bog. These aerobic bacteria efficiently reduced Se(IV) with intracellular reduced Se0 observed in the cytoplasm under dark aerobic conditions. The proteome analysis of Se(IV) supplement and temperature responses by SDS-PAGE gel electrophoresis showed variations in the protein expression on the 40–60 kDa regions following these stress factors, probably through enzymes associated to oxidative stress or temperature adaptation. NO3/NO2/SO42− addition enhanced Se(IV) uptake in both bacteria, but Se(IV) uptake sustained also under sulphur and nitrogen starvation. Our findings suggest two different transport mechanisms for Se(IV) uptake in these Pseudomonas sp. strains; a low affinity transport system up-regulated by NO3/NO2/SO42− and a distinct Se(IV)O32− regulated transport system. Following transport, Se(IV) is reduced in the cytoplasm, forming Se0 granules, visible in TEM and verified using EDX.

    Citation: Merja Lusa, Jenna Knuutinen, Malin Bomberg. Uptake and reduction of Se(IV) in two heterotrophic aerobic Pseudomonads strains isolated from boreal bog environment[J]. AIMS Microbiology, 2017, 3(4): 798-814. doi: 10.3934/microbiol.2017.4.798

    Related Papers:

  • Selenite (Se(IV), SeO32−) uptake and the effect of selenite supplement on protein synthesis was investigated in two Pseudomonas sp. strains isolated from a boreal bog. These aerobic bacteria efficiently reduced Se(IV) with intracellular reduced Se0 observed in the cytoplasm under dark aerobic conditions. The proteome analysis of Se(IV) supplement and temperature responses by SDS-PAGE gel electrophoresis showed variations in the protein expression on the 40–60 kDa regions following these stress factors, probably through enzymes associated to oxidative stress or temperature adaptation. NO3/NO2/SO42− addition enhanced Se(IV) uptake in both bacteria, but Se(IV) uptake sustained also under sulphur and nitrogen starvation. Our findings suggest two different transport mechanisms for Se(IV) uptake in these Pseudomonas sp. strains; a low affinity transport system up-regulated by NO3/NO2/SO42− and a distinct Se(IV)O32− regulated transport system. Following transport, Se(IV) is reduced in the cytoplasm, forming Se0 granules, visible in TEM and verified using EDX.


    加载中
    [1] Helin J, Hjerpe T, Ikonen ATK (2010) Review of element specific data for biosphere assessment BSA-2009. Working Report 2010-37, Posiva Oy.
    [2] Manceau A, Gallup DL (1997) Removal of selenocyanate in water by precipitation: characterization of copper-selenium precipitate by x-ray diffraction, infrared, and x-ray adsorption spectroscopy. Environ Sci Technol 31: 968–976. doi: 10.1021/es960138a
    [3] de Souza MP, Chu D, Zhao M, et al. (1999) Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol 119: 565–573. doi: 10.1104/pp.119.2.565
    [4] Sharmasarkar S, Vance GF (2002) Soil and plant selenium at a reclaimed uranium mine. J Environ Qual 31: 1516–1521. doi: 10.2134/jeq2002.1516
    [5] Coppin F, Charboullet C, Martin-Garin A (2009). Selenite interactions with some particulate organic and mineral fractions isolated from a natural grassland soil. Eur J Soil Sci 60: 369–376. doi: 10.1111/j.1365-2389.2009.01127.x
    [6] Deverel SJ, Fio JL, Dubrovsky NM (1994) Distribution and mobility of selenium in groundwater in the western San Joaquin Valley of California, In: Frankenberger WT, Benson S, Editors, Selenium in the environment, New York: Marcel Dekker, Inc., 157–184.
    [7] Mayland HF (1994) Selenium in plant and animal nutrition, In: Frankenberger WT, Benson S, Editors, Selenium in the environment, New York: Marcel Dekker, Inc., 29–46.
    [8] Tokunga TK, Zawislanski PT, Johannis PW, et al. (1994) Field investigations of selenium speciation, transformation and transport in soils from Kesterson Reservoir and Lahontan Valley, In: Frankenberger WT, Benson S, Editors, Selenium in the environment, New York: Marcel Dekker, 119–138.
    [9] Barceloux DG (1999) Selenium. J Toxicol Clin Toxicol 37: 145–172.
    [10] Terry N, Zayed AM, de Souza MP, et al. (2000) Selenium in higher plants. Annu Rev Plant Physiol 51: 401–432.
    [11] Bébien M, Chauvin JP, Adriano JM, et al. (2001) Effect of selenite on growth and protein synthesis in the phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microb 67: 4440–4447. doi: 10.1128/AEM.67.10.4440-4447.2001
    [12] Tarze A, Dauplais M, Grigoras I, et al. (2007) Extracellular production of hydrogen selenide accounts for thiol-assisted toxicity of selenite against Saccharomyces Cerevisiae. J Biol Chem 282: 8759–8767. doi: 10.1074/jbc.M610078200
    [13] Kramer GF, Ames BS (1988) Mechanisms of mutagenicity and toxicity of sodium selenite in Salmonella typhimurium. Mutat Res 201: 169–180. doi: 10.1016/0027-5107(88)90123-6
    [14] Oremland RS, Steinberg N, Maest AS, et al. (1990) Measurement of in situ rates of selenate removal by dissimilatory bacterial reduction in sediments. Environ Sci Technol 32: 3749–3755.
    [15] Zhang Y, Moore JM (1996) Selenium fractionation and speciation in a wetland system. Environ Sci Technol 30: 2613–2619. doi: 10.1021/es960046l
    [16] Stolz JF, Oremland RS (1999) Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23: 615–627. doi: 10.1111/j.1574-6976.1999.tb00416.x
    [17] Charlet L, Scheinost AC, Tournassat C, et al. (2007) Electron transfer at the mineral/water interface: Selenium reduction on by ferrous iron sorbed on clay. Geochim Cosmochim Ac 71: 5731–5749.
    [18] Macy JM, Michel TA, Kirsch DG (1989) Selenate reduction by a Pseudomonas species: a new mode of anaerobic respiration. FEMS Microbiol Lett 61: 195–198. doi: 10.1111/j.1574-6968.1989.tb03577.x
    [19] Oremland RS, Hollibaugh JT, Maest AS, et al. (1989) Selenate reduction to elemental selenium by anaerobic bacteria in sediments and culture: biogeochemical significance of a novel, sulfate-independent respiration. Appl Environ Microb 55: 2333– 2343.
    [20] Kessi JM, Ramuz E, Wehrli M, et al. (1999) Reduction of selenite and detoxification of elemental selenium by the phototropic bacterium Rodospirillum rubrum. Appl Environ Microb 65: 4737–4740.
    [21] Roux MG, Sarret I, Pignot-Paintrand M, et al. (2001) Mobilization of selenite by Ralstonia metallidurans CH34. Appl Environ Microb 67: 769–773. doi: 10.1128/AEM.67.2.769-773.2001
    [22] Oremland RS, Herbel MJ, Blum JS, et al. (2004) Structural and spectral features of selenium nanospheres produced by Se-respiring bacteria. Appl Environ Microb 70: 52–60. doi: 10.1128/AEM.70.1.52-60.2004
    [23] Sarret GL, Avoscan L, Carriere M, et al. (2005) Chemical forms of selenium in the metal resistant bacterium Ralstonia metallidurans CH34 exposed to selenite and selenate. Appl Environ Microb 71: 2331–2337. doi: 10.1128/AEM.71.5.2331-2337.2005
    [24] Nelson DC, Casey WH, Sison JD, et al. (1996) Selenium uptake by sulphur-accumulating bacteria. Geochim Cosmochim Ac 60: 3531–3539.
    [25] Li DB, Cheng YY, Wu C, et al. (2014) Selenite reduction by Shewanella oneidensis MR-1 is mediated by fumarate reductase in periplasm. Sci Rep 4: 3735.
    [26] Losi ME, Frankenberger WT (1997) Reduction of selenium oxyanions by Enterobacter cloacae SLD1a-1: isolation and growth of the bacterium and its expulsion of selenium particles. Appl Environ Microb 63: 3079–3084.
    [27] Yee N, Ma J, Dalia A, et al. (2007) Se(VI) reduction and the precipitation of Se(0) by the facultative bacterium Enterobacter cloacae SLD1a-1 are regulated by FNR. Appl Environ Microb 73: 1914–1920. doi: 10.1128/AEM.02542-06
    [28] Lusa M, Bomberg M, Aromaa H, et al. (2015) The microbial impact on the sorption behaviour of selenite in an acidic, nutrient-poor boreal bog. J Environ Radioactiv 147: 85–96. doi: 10.1016/j.jenvrad.2015.05.014
    [29] Lusa M, Lehto J, Aromaa H, et al. (2016) The uptake of radioiodide by Paenibacillus sp., Pseudomonas sp., Burkholderia sp. and Rhodo-coccus sp. isolated from a boreal nutrient-poor bog. J Environ Sci 44: 26–37.
    [30] Dereeper A, Guignon V, Blanc G, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465–W469.
    [31] Dereeper A, Audic S, Claverie JM, et al. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10: 8. doi: 10.1186/1471-2148-10-8
    [32] Turner RJ, Weiner JH, Taylor DE (1998) Selenium metabolism in Escherichia coli. Biometals 11: 223–227.
    [33] Heider J, Bröck A (1993) Selenium metabolism in microorganisms. Adv Microb Physiol 35: 71–109. doi: 10.1016/S0065-2911(08)60097-1
    [34] Macy JM, Rech S, Auling G, et al. (1993) Thauera selenatis gen. nov., sp. nov., a member of the beta subclass of Proteobacteria with a novel type of anaerobic respiration. Int J Syst Evol Micr 43: 135–142.
    [35] Gharieb MM, Gadd GM (2004) The kinetics of 75[Se]-selenite uptake by Saccharomyces cerevisiae and the vacuolization response to high concentrations. Mycol Res 108: 1415–1422. doi: 10.1017/S0953756204001418
    [36] Kari C, Nagy Z, Kovácz P, et al. (1971) Mechanism of the growth inhibitory effect of cysteine on Escherichia coli. J Gen Microbiol 68: 349–356.
    [37] Harrison G, Curle C, Laishley EJ (1984) Purification and characterization of an inducible dissimilatory type sulfite reductase from Clostridium pasteurianum. Arch Microbiol 138: 72–78. doi: 10.1007/BF00425411
    [38] DeMoll-Decker H, Macy JM (1993) The periplasmic nitrite reductase of Thauera selenatis may catalyze the reduction of selenite to elemental selenium. Arch Microbiol 160: 241–247.
    [39] Hudman JF, Glenn AR (1984) Selenite uptake and incorporation by Selenomonas ruminantium. Arch Microbiol 140: 252–256. doi: 10.1007/BF00454937
    [40] Brown TA, Shrift A (1980) Assimilation of selenate and selenite by Salmonella typhimurium. Can J Microbiol 26: 671–675. doi: 10.1139/m80-117
    [41] Smith FW, Hawkesford MJ, Prosser IM, et al. (1995) Isolation of cDNA from Saccharomyces cerevisiae that encodes a high-affinity sulfate transporter at the plasma membrane. Mol Gen Genet 247: 709–715. doi: 10.1007/BF00290402
    [42] Guzzo J, Dubow MS (2000) A novel selenite- and tellurite-inducible gene in Escherichia coli. Appl Environ Microb 66: 4972–4978. doi: 10.1128/AEM.66.11.4972-4978.2000
    [43] Yamada A, Miyashita M, Inoue K, et al. (1997) Extracellular reduction of selenite by a novel marine photosynthetic bacterium. Appl Microbiol Biotechnol 48: 367–372. doi: 10.1007/s002530051064
    [44] Bryant RD, Laishley EJ (1988) Evidence for two transporters of sulfur and selenium oxyanions in Clostridium pasteurianum. Can J Microbiol 34: 700–703. doi: 10.1139/m88-118
    [45] Hartke A, Bouche S, Laplace JM, et al. (1995) UV-inducible proteins and UV-induced cross-protection against acid, ethanol, H2O2 or heat treatments in Lactococcus lactis subsp. lactis. Arch Microbiol 163: 329–336. doi: 10.1007/BF00404205
    [46] Nepple BB, Bachofen R (1997) Induction of stress proteins in the phototrophic bacterium Rhodobacter sphaeroides. FEMS Microbiol Lett 153: 173–180. doi: 10.1111/j.1574-6968.1997.tb10479.x
    [47] Keto-Timonen R, Hietala N, Palonen E, et al. (2016) Cold shock proteins: A minireview with special emphasis on Csp-family of enteropathogenic Yersinia. Front Microbiol 7.
    [48] Van FV, Chasteen TG, Pickering IJ, et al. (2000) Fate of selenate and selenite metabolized by Rhodobacter sphaeroides. Appl Environ Microb 66: 4849–4853. doi: 10.1128/AEM.66.11.4849-4853.2000
  • Reader Comments
  • © 2017 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(4581) PDF downloads(939) Cited by(6)

Article outline

Figures and Tables

Figures(8)  /  Tables(1)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog