Current Microbiology

, Volume 69, Issue 3, pp 374–380 | Cite as

Potential Application in Mercury Bioremediation of a Marine Sponge-Isolated Bacilluscereus strain Pj1

  • Juliana F. Santos-Gandelman
  • Kimberly Cruz
  • Sharron Crane
  • Guilherme Muricy
  • Marcia Giambiagi-deMarval
  • Tamar Barkay
  • Marinella S. Laport
Article

Abstract

Sponges are sessile marine invertebrates that can live for many years in the same location, and therefore, they have the capability to accumulate anthropogenic pollutants such as metals over a long period. Almost all marine sponges harbor a large number of microorganisms within their tissues. The Bacilluscereus strain Pj1 was isolated from a marine sponge, Polymastia janeirensis, and was found to be resistant to 100 μM HgCl2 and to 10 μM methylmercury (MeHg). Pj1 was also highly resistant to other metals, including CdCl2 and Pb(NO3)2, alone or in combination. The mer operon was located on the bacterial chromosome, and the volatilization test indicated that the B. cereus Pj1 was able to reduce Hg2+–Hg0. Cold vapor atomic absorption spectrometry demonstrated that Pj1 volatilized 80 % of the total MeHg that it was exposed to and produced elemental Hg when incubated with 1.5 μM MeHg. Pj1 also demonstrated sensitivity to all antibiotics tested. In addition, Pj1 demonstrated a potential for biosurfactant production, presenting an emulsification activity better than synthetic surfactants. The results of this study indicate that B.cereus Pj1 is a strain that can potentially be applied in the bioremediation of HgCl2 and MeHg contamination in aquatic environments.

References

  1. 1.
    Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14(4):176–182PubMedCrossRefGoogle Scholar
  2. 2.
    Ball MM, Carrero P, Castro D, Yarzábal A (2007) Mercury resistance in bacterial strains isolated from tailing ponds in a gold mining area near El Callao (Bolívar State, Venezuela). Curr Microbiol 54:149–154PubMedCrossRefGoogle Scholar
  3. 3.
    Barkay T, Wagner-Döbler I (2005) Microbial transformations of mercury: potentials, challenges, and achievements in controlling mercury toxicity in the environment. Adv Appl Microbiol 57:1–52PubMedCrossRefGoogle Scholar
  4. 4.
    Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance: from atoms to ecosystems. FEMS Microbiol Rev 27:355–384PubMedCrossRefGoogle Scholar
  5. 5.
    Boyd ES, Barkay T (2012) The mercury resistance operon: from an origin in a geothermal environment to an efficient detoxification machine. Front Microbiol 3:349PubMedCentralPubMedGoogle Scholar
  6. 6.
    Calderon J, Ortiz-Perez D, Yanez L, Diaz-Barriga F (2003) Human exposure to metals. Pathways of exposure, biomarkers of effect and host factors. Ecotoxicol Environ Saf 56:93–103PubMedCrossRefGoogle Scholar
  7. 7.
    Carillo P, Mardarz C, Pitta-Alvarez S (1996) Isolation and selection of biosurfactant producing bacteria. World J Microbiol Biotechnol 12:82–84CrossRefGoogle Scholar
  8. 8.
    Chang JS, Hong J, Ogunseitan OA, Olson HB (1993) Interaction of mercuric ions with the bacterial growth medium and its effects in enzymatic reduction of mercury. Biotechnol Prog 9:526–532CrossRefGoogle Scholar
  9. 9.
    Clinical and Laboratory Standards Institute (CLSI) (2013) Performance standards for antimicrobial susceptibility testing, 23th informational supplement M100-S23. CLSI, WayneGoogle Scholar
  10. 10.
    Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53(2):224–229PubMedCentralPubMedGoogle Scholar
  11. 11.
    De J, Ramaiah N, Mesquita A, Verlekar XN (2003) Tolerance to various toxicants by marine bacteria highly resistant to mercury. Mar Biotechnol 5(2):185–193PubMedCrossRefGoogle Scholar
  12. 12.
    De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10(4):471–477PubMedCrossRefGoogle Scholar
  13. 13.
    Gadd GM, White C (1993) Microbial treatment of metal pollution: a working biotechnology? Trends Biotechnol 11:353–359PubMedCrossRefGoogle Scholar
  14. 14.
    Hardoim C, Costa R, Araújo F, Hadju E, Peixoto RS, Lins U et al (2009) Microbial diversity in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl Environ Microbiol 75:3331–3343PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Li J, Zhang L, Wu Y, Liu Y, Zhou P, Wen S et al (2009) A national survey of polychlorinated dioxins, furans (PCDD/Fs) and dioxin-like polychlorinated biphenyls (DL-PCBs) in human milk in China. Chemosphere 75:1236–1242PubMedCrossRefGoogle Scholar
  16. 16.
    Liebert CA, Wireman J, Smith T, Summers AO (1997) Phylogeny of mercury resistance (mer) operons of Gram-negative bacteria isolated from the fecal flora of primates. Appl Environ Microbiol 63:1066–1076PubMedCentralPubMedGoogle Scholar
  17. 17.
    Maldonado M, Carmona M, Velásquez Z, Puig A, Cruzado A, López A, Young CM (2005) Siliceous sponges as a silicon sink: an overlooked aspect of benthopelagic coupling in the marine silicon cycle. Limnol Oceanogr 50(3):799–809CrossRefGoogle Scholar
  18. 18.
    Marinho PR, Moreira APB, Pellegrino FLPC, Muricy G, Bastos MCF, Dos Santos KRN, Giambiagi-deMarval M, Laport MS (2009) Marine Pseudomonas putida: a potential source of antimicrobial substances against antibiotic-resistant bacteria. Mem Inst Oswaldo Cruz 104:678–682PubMedCrossRefGoogle Scholar
  19. 19.
    Muricy G, Hadju E (2006) Porifera Brasilis: Guia de Identificação das Esponjas Mais Comuns do Sudeste do Brasil. Eclesiarte, Rio de JaneiroGoogle Scholar
  20. 20.
    Murtaza I, Dutt A, Mushtaq D, Ali A (2005) Molecular cloning and genetic analysis of functional merB gene from Indian isolates of Escherichia coli. Curr Microbiol 51:297–302PubMedCrossRefGoogle Scholar
  21. 21.
    Nakamura K, Nakahara H (1988) Simplified X-ray film method for detection of bacterial volatilization of mercury chloride by Escherichia coli. Appl Environ Microbiol 54:2871–2873PubMedCentralPubMedGoogle Scholar
  22. 22.
    Nascimento AMA, Chartone-Souza E (2003) Operon mer: bacterial resistance to mercury and potential for bioremediation of contaminated environments. Genet Mol Res 2(1):92–101PubMedGoogle Scholar
  23. 23.
    Pepi M, Gaggi C, Bernardini E, Focardi S, Lobianco A, Ruta M, Nicolardi V et al (2010) Mercury-resistant bacterial strains Pseudomonas and Psychrobacter spp. isolated from sediments of Orbetello Lagoon (Italy) and their possible use in bioremediation processes. Int Biodeterior Biodegrad 65:85–91CrossRefGoogle Scholar
  24. 24.
    Santos OCS, Pontes PVML, Santos JFM, Muricy G, Giambiagi-deMarval M, Laport MS (2010) Isolation, characterization and phylogeny of sponge-associated bacteria with antimicrobial activities from Brazil. Res Microbiol 161(7):604–612PubMedCrossRefGoogle Scholar
  25. 25.
    Santos-Gandelman JF, Santos OC, Pontes PV, Andrade CL, Korenblum E, Muricy G, Giambiagi-deMarval M, Laport MS (2013) Characterization of cultivable bacteria from Brazilian sponges. Mar Biotechnol (NY) 15(6):668–676CrossRefGoogle Scholar
  26. 26.
    Selvin J, Shanmugha-Priya S, Seghal-Kiran G, Thangavelu T, Sapna-Bai N (2009) Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiol Res 164:352–363PubMedCrossRefGoogle Scholar
  27. 27.
    Turque AS, Cardoso AM, Silveira CB, Vieira RP, Freitas FAD, Albano RM et al (2008) Bacterial communities of the marine sponges Hymeniacidon heliophila and Polymastia janeirensis and their environment in Rio de Janeiro, Brazil. Mar Biol 155(2):135–146CrossRefGoogle Scholar
  28. 28.
    Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208PubMedCrossRefGoogle Scholar
  29. 29.
    Vetriani C, Chew YS, Miller SM, Yagi J, Coombs J, Lutz RA, Barkay T (2005) Mercury adaptation among bacteria from a deepsea hydrothermal vent. Appl Environ Microbiol 71:220–226PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Wang Y, Boyd E, Crane S, Lu-Irving P, Krabbenhoft D, King S et al (2011) Environmental conditions constrain the distribution and diversity of Archaeal merA in Yellowstone National Park, Wyoming, U.S.A. Microb Ecol 62(4):739–752PubMedCrossRefGoogle Scholar
  31. 31.
    Wiatrowski HA, Ward PM, Barkay T (2006) Novel reduction of mercury(II) by mercury-sensitive dissimilatory metal reducing bacteria. Environ Sci Technol 40:6690–6696PubMedCrossRefGoogle Scholar
  32. 32.
    World Health Organization (2000) Air quality guidelines for Europe. In: WHO regional publication European series, vol 91:V-S. Copenhagen, pp 1–273Google Scholar
  33. 33.
    Youssef NH, Duncan KE, Nagle DD, Savage KH, Knapp RM, McInerney MJ (2004) Comparison of methods to detect biosurfactant production by diverse microorganisms. J Microbiol Methods 56:339–347PubMedCrossRefGoogle Scholar
  34. 34.
    Zhang W, Chen L, Liu D (2011) Characterization of a marine-isolated mercury-resistant Pseudomonas putida strain SP1 and its potential application in marine mercury reduction. Appl Microbiol Biotechnol 93(3):1305–1314PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Juliana F. Santos-Gandelman
    • 1
  • Kimberly Cruz
    • 2
  • Sharron Crane
    • 2
  • Guilherme Muricy
    • 3
  • Marcia Giambiagi-deMarval
    • 1
  • Tamar Barkay
    • 2
  • Marinella S. Laport
    • 1
  1. 1.Instituto de Microbiologia Paulo de GóesUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Department of Biochemistry and Microbiology, Cook CollegeRutgers UniversityNew BrunswickUSA
  3. 3.Museu NacionalUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil

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