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Bioaccumulation of Vanadium by Vanadium-Resistant Bacteria Isolated from the Intestine of Ascidia sydneiensis samea

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Abstract

Isolation of naturally occurring bacterial strains from metal-rich environments has gained popularity due to the growing need for bioremediation technologies. In this study, we found that the vanadium concentration in the intestine of the vanadium-rich ascidian Ascidia sydneiensis samea could reach 0.67 mM, and thus, we isolated vanadium-resistant bacteria from the intestinal contents and determined the ability of each bacterial strain to accumulate vanadium and other heavy metals. Nine strains of vanadium-resistant bacteria were successfully isolated, of which two strains, V-RA-4 and S-RA-6, accumulated vanadium at a higher rate than did the other strains. The maximum vanadium absorption by these bacteria was achieved at pH 3, and intracellular accumulation was the predominant mechanism. Each strain strongly accumulated copper and cobalt ions, but accumulation of nickel and molybdate ions was relatively low. These bacterial strains can be applied to protocols for bioremediation of vanadium and heavy metal toxicity.

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References

  • Antipov AN, Lyalikova NN, Khijniak TV, L’vov NP (1998) Molybdenum-free nitrate reductases from vanadate-reducing bacteria. FEBS Lett 441:257–260

    Article  CAS  PubMed  Google Scholar 

  • Antipov AN, Lyalikova NN, L’vov NP (2000) Vanadium-binding protein excreted by vanadate-reducing bacteria. IUBMB Life 49:137–141

    Article  CAS  PubMed  Google Scholar 

  • Atlas RM (2005) Handbook of media for environmental microbiology. doi:10.1201/9781420037487

  • Behrendt L, Larkum AWD, Trampe E et al (2012) Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella. ISME J 6:1222–1237

    Article  CAS  PubMed  Google Scholar 

  • Bisconti L, Pepi M, Mangani S, Baldi F (1997) Reduction of vanadate to vanadyl by a strain of Saccharomyces cerevisiae. Biometals 10:239–246

    Article  CAS  PubMed  Google Scholar 

  • Blasiak LC, Zinder SH, Buckley DH, Hill RT (2014) Bacterial diversity associated with the tunic of the model chordate Ciona intestinalis. ISME J 8:309–320

    Article  CAS  PubMed  Google Scholar 

  • Bowman BJ (1983) Vanadate uptake in Neurospora crassa occurs via phosphate transport system II. J Bacteriol 152:286

    Google Scholar 

  • Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269

    Article  CAS  PubMed  Google Scholar 

  • Carpentier W, Sandra K, De Smet I et al (2003) Microbial reduction and precipitation of vanadium by Shewanella oneidensis. Appl Environ Microbiol 69:3636–3639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carpentier W, De Smet L, Van Beeumen J et al (2005) Respiration and growth of Shewanella oneidensis MR-1 using vanadate as the sole electron acceptor. J Bacteriol 187: 3293–3301

  • da Silva SG, Gillan DC, Dubilier N, De Ridder C (2006) Characterization by 16S rRNA gene analysis and in situ hybridization of bacteria living in the hindgut of a deposit-feeding echinoid (Echinodermata). J Mar Biol Assoc UK 86:1209–1213

    Article  Google Scholar 

  • Desaunay A, Martins JMF (2014) Comparison of chemical washing and physical cell-disruption approaches to assess the surface adsorption and internalization of cadmium by Cupriavidus metallidurans CH34. J Hazard Mater 273:231–238

    Article  CAS  PubMed  Google Scholar 

  • Dishaw LJ, Flores-Torres J, Lax S et al (2014) The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS One 9:e93386

    Article  PubMed  PubMed Central  Google Scholar 

  • Esposito A, Pagnanelli F, Vegliâ F (2002) pH-related equilibria models for biosorption in single metal systems. Chem Eng Sci 57:307–313

    Article  CAS  Google Scholar 

  • Faury N, Saulnier D, Thompson FL et al (2004) Vibrio crassostreae sp. nov., isolated from the haemolymph of oysters (Crassostrea gigas). Int J Syst Evol Microbiol 54:2137–2140

    Article  CAS  PubMed  Google Scholar 

  • Finnegan L, Garcia-Melgares M, Gmerek T et al (2011) A survey of culturable aerobic and anaerobic marine bacteria in de novo biofilm formation on natural substrates in St. Andrews Bay, Scotland. Antonie Van Leeuwenhoek 100:399–404

    Article  PubMed  Google Scholar 

  • Ghazvini PTM, Mashkani SG (2009) Effect of salinity on vanadate biosorption by Halomonas sp. GT-83: preliminary investigation on biosorption by micro-PIXE technique. Bioresour Technol 100:2361–2368

    Article  CAS  Google Scholar 

  • Hansen GH, Sørheim R (1991) Improved method for phenotypical characterization of marine bacteria. J Microbiol Methods 13:231–241

    Article  Google Scholar 

  • Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25:195–231

    Article  CAS  PubMed  Google Scholar 

  • Henderson G, Evans IH, Bruce IJ (1989) The effects of vanadate on the yeast Saccharomyces cerevisiae. Antonie Van Leeuwenhoek 55:99–107

    Article  CAS  PubMed  Google Scholar 

  • Hernández A, Mellado RP, Martínez JL, Herna A (1998) Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae. Appl Environ Microbiol 64:4317–4320

    PubMed  PubMed Central  Google Scholar 

  • Hooper LV, Wong MH, Thelin A et al (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Guo C-L, Lu G-N et al (2014) Bioaccumulation characterization of cadmium by growing Bacillus cereus RC-1 and its mechanism. Chemosphere 109:134–142

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Sawabe T, Zhukova NV et al (2003) Occurrence and diversity of mesophilic Shewanella strains isolated from the North-West Pacific Ocean. Syst Appl Microbiol 26:293–301

    Article  CAS  PubMed  Google Scholar 

  • Jayasree L, Janakiram P, Madhavi R (2006) Characterization of Vibrio spp. associated with diseased shrimp from culture ponds of Andhra Pradesh (India). J World Aquacult Soc 37:523–532

    Article  Google Scholar 

  • Jiang H, Dong H, Ji S (2007) Microbial diversity in the deep marine sediments from the Qiongdongnan basin in South China Sea. Geomicrobiol J 24:505–517

    Article  CAS  Google Scholar 

  • Kamika I, Momba MNB (2014) Microbial diversity of emalahleni mine water in South Africa and tolerance ability of the predominant organism to vanadium and nickel. PLoS One 9:e86189

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanda T, Nose Y, Wuchiyama J et al (1997) Identification of a vanadium-associated protein from the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 14:37–42

    Article  CAS  PubMed  Google Scholar 

  • Kanik-ennulat C, Neff N (1990) Vanadate-resistant mutants of Saccharomyces cerevisiae show alterations in protein phosphorylation and growth control. Mol Cell Biol 10:898–909

  • Kanik-ennulat C, Montalvo E, Neff N (1995) Sodium orthovanadate-resistant mutants of Saccharomyces cerevisiae show defects in Golgi-mediated protein glycosylation, sporulation and detergent resistance. Genetics 140:933–943

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaschak E, Knopf B, Petersen JH et al (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

    Article  CAS  Google Scholar 

  • Kawakami N, Ueki T, Matsuo K et al (2006) Selective metal binding by Vanabin2 from the vanadium-rich ascidian, Ascidia sydneiensis samea. Biochim Biophys Acta 1760:1096–1101

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li P, Burr GS, Gatlin DM III et al (2007) Dietary supplementation of short-chain fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of pacific white shrimp, Litopenaeus vannamei, cultured in a recirculating system. J Nutr 137:2763–2768

    CAS  PubMed  Google Scholar 

  • López A, Lázaro N, Priego JM, Marqués AM (2000) Effect of pH on the biosorption of nickel and other heavy metals by Pseudomonas fluorescens 4F39. J Ind Microbiol Biotechnol 24:146–151

    Article  Google Scholar 

  • Maruyama A, Mita N, Higashihara T (1993) Particulate materials and microbial assemblages around the lzena black smoking vent in the Okinawa trough. J Oceanogr 49:353–367

    Article  CAS  Google Scholar 

  • Michibata HE (2012) Vanadium. Springer, Dordrecht

    Book  Google Scholar 

  • Michibata H, Iwata Y, Hirata J (1991) Isolation of highly acidic and vanadium-containing blood cells from among several types of blood cell from ascidiidae species by density-gradient centrifugation. J Exp Zool 257:306–313

    Article  Google Scholar 

  • Myers JM, Antholine WE, Myers CR (2004) Vanadium (V) reduction by Shewanella oneidensis MR-1 requires menaquinone and cytochromes from the cytoplasmic and outer membranes. Appl Environ Microbiol 70:1405–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Bernad I, Anderson RT, Vrionis HA, Lovley DR (2004) Vanadium respiration by Geobacter metallireducens: novel strategy for in situ removal of vanadium from groundwater. Appl Environ Microbiol 70:3091–3095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pabst MW, Miller CD, Dimkpa CO et al (2010) Defining the surface adsorption and internalization of copper and cadmium in a soil bacterium, Pseudomonas putida. Chemosphere 81:904–910

    Article  CAS  PubMed  Google Scholar 

  • Romalde JL, Diéguez AL, Lasa A, Balboa S (2014) New Vibrio species associated to molluscan microbiota: a review. Front Microbiol 4:1–11

    Article  Google Scholar 

  • Rungrassamee W, Klanchui A, Maibunkaew S, Chaiyapechara S (2014) Characterization of intestinal bacteria in wild and domesticated adult black tiger shrimp (Penaeus monodon). PLoS One 9:e91853

    Article  PubMed  PubMed Central  Google Scholar 

  • Samino S, Michibata H, Ueki T (2012) Identification of a novel vanadium-binding protein by EST analysis on the most vanadium-rich ascidian, Ascidia gemmata. Mar Biotechnol (NY) 14:143–154

    Article  CAS  Google Scholar 

  • Shirdam R, Khanafari A, Tabatabaee A (2006) Cadmium, nickel and vanadium accumulation by three strains of marine bacteria. Iran J Biotechnol 4:180–187

    CAS  Google Scholar 

  • Silver S (1996) Bacterial resistances to toxic metal ions—a review. Gene 179:9–19

    Article  CAS  PubMed  Google Scholar 

  • Simon CA, McQuaid C (1999) Extracellular digestion in two co-occurring intertidal mussels (Perna perna (L.) and Choromytilus meridionalis (Kr)) and the role of enteric bacteria in their digestive ecology. J Exp Mar Biol Ecol 234:59–81

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka R, Ootsubo M, Sawabe T et al (2004) Biodiversity and in situ abundance of gut microflora of abalone (Haliotis discus hannai) determined by culture-independent techniques. Aquaculture 241:453–463

    Article  Google Scholar 

  • Thompson FL, Thompson CC, Swings J (2003) Vibrio tasmaniensis sp. nov., isolated from Atlantic Salmon (Salmo salar L.). Syst Appl Microbiol 26:65–69

    Article  CAS  PubMed  Google Scholar 

  • Thorsen MS (1999) Abundance and biomass of the gut-living microorganisms (bacteria, protozoa and fungi) in the irregular sea urchin Echinocardium cordatum (Spatangoida: Echinodermata). Mar Biol 133:353–360

    Article  Google Scholar 

  • Ueki T, Michibata H (2011) Molecular mechanism of the transport and reduction pathway of vanadium in ascidians. Coord Chem Rev 255:2249–2257

    Article  CAS  Google Scholar 

  • Ueki T, Adachi T, Kawano S et al (2003a) Vanadium-binding proteins (vanabins) from a vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta Gene Struct Expr 1626:43–50

    Article  CAS  Google Scholar 

  • Ueki T, Sakamoto Y, Yamaguchi N, Michibata H (2003b) Bioaccumulation of copper ions by Escherichia coli expressing vanabin genes from the vanadium-rich ascidian Ascidia sydneiensis samea. Appl Environ Microbiol 69(11):6442–6446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueki T, Shintaku K, Yonekawa Y et al (2007) Identification of Vanabin-interacting protein 1 (VIP1) from blood cells of the vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1770:951–957

    Article  CAS  PubMed  Google Scholar 

  • Ueki T, Yamaguchi N, Romaidi et al (2014) Vanadium accumulation in ascidians: a system overview. Coord Chem Rev 301–302: 300–308

  • van Marwijk J, Opperman DJ, Piater LA, van Heerden E (2009) Reduction of vanadium(V) by Enterobacter cloacae EV-SA01 isolated from a South African deep gold mine. Biotechnol Lett 31:845–849

    Article  CAS  PubMed  Google Scholar 

  • Willsky GR, Leung J, Offermann PV, Plotnick EK (1985) Isolation and characterization of vanadate-resistant mutants of Saccharomyces cerevisiae. J Bacteriol 164:611–617

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi N, Kamino K, Ueki T, Michibata H (2004) Expressed sequence tag analysis of vanadocytes in a vanadium-rich ascidian, Ascidia sydneiensis samea. Mar Biotechnol (NY) 6:165–174

    Article  CAS  Google Scholar 

  • Yoshinaga M, Ueki T, Michibata H (2007) Metal binding ability of glutathione transferases conserved between two animal species, the vanadium-rich ascidian Ascidia sydneiensis samea and the schistosome Schistosoma japonicum. Biochim Biophys Acta 1770:1413–1418

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Dong H, Zhao L et al (2014) Microbial reduction and precipitation of vanadium by mesophilic and thermophilic methanogens. Chem Geol 370:29–39

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to thank the staff at Kojima Port, Okayama, Japan, for their help in collecting adult ascidians and Dr. N. Yamaguchi for his help in collecting and maintaining adult ascidians. DNA sequencing analyses were done at the Natural Science Center for Basic Research and Development (N-BARD), Hiroshima University. This work was partly supported by Grants-in-Aid from JSPS (Nos. 25120508 and 25440170) and an Environmental Research Grant from the Nippon Life Insurance Foundation (2012). R. is supported by the Directorate of Islamic Higher Education, Ministry of Religious Affairs (MORA), Republic of Indonesia.

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  1. Molecular Physiology Laboratory, Graduate School of Science, Hiroshima University, Higashi-Hiroshima, Japan

    Romaidi & Tatsuya Ueki

  2. Marine Biological Laboratory, Graduate School of Science, Hiroshima University, Onomichi, Japan

    Tatsuya Ueki

  3. Biology Department, Science and Technology Faculty, State Islamic University of Malang, Malang, Indonesia

    Romaidi

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Correspondence to Tatsuya Ueki.

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Romaidi, Ueki, T. Bioaccumulation of Vanadium by Vanadium-Resistant Bacteria Isolated from the Intestine of Ascidia sydneiensis samea . Mar Biotechnol 18, 359–371 (2016). https://doi.org/10.1007/s10126-016-9697-5

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