Abstract
Both point and non-point sources increase the pollution status of mercury and increase the population of mercury-resistant marine bacteria (MRMB). They can be targeted as the indicator organism to access marine mercury pollution, besides utilization in bioremediation. Thus, sediment and water samples were collected for 2 years (2010–2012) along Odisha coast of Bay of Bengal, India. Mercury content of the study sites varied from 0.47 to 0.99 ppb irrespective of the seasons of sampling. A strong positive correlation was observed between mercury content and MRMB population (P < 0.05) suggesting the utilization of these bacteria to assess the level of mercury pollution in the marine environment. Seventy-eight percent of the MRMB isolates were under the phylum Firmicutes, and 36 and 31 % of them could resist mercury by mer operon–mediated volatilization and mercury biosorption, respectively. In addition, most of the isolates could resist a number of antibiotics and toxic metals. All the MRMB isolates possess the potential of growth and survival at cardinal pH (4–8), temperature (25–37 °C), and salinity (5–35 psu). Enterobacteria repetitive intergenic consensus (ERIC) and repetitive element palindromic PCR (REP-PCR) produced fingerprints corroborating the results of 16S rRNA gene sequencing. Fourier transform infrared (FTIR) spectral analysis also revealed strain-level speciation and phylogenetic relationships.
Similar content being viewed by others
References
Akoachere JFTK, Oben PM, Mbivnjo BS, Ndip LM, Nkwelang G, Ndip RN (2008) Bacterial indicators of pollution of the Douala lagoon, Cameroon: public health implications. Afr Health Sci 8:85–89
Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384
Bauer A, Kirby W, Sherris J, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496
Bayramoğlu G, Tuzun I, Celik G, Yilmaz M, Arica MY (2006) Biosorption of mercury(II), cadmium(II) and lead(II) ions from aqueous system by microalgae Chlamydomonas reinhardtii immobilized in alginate beads. Int J Miner Process 81:35–43
Becker K, Al Laham N, Fegeler W, Proctor RA, Peters G, von Eiff C (2006) Fourier-transform infrared spectroscopic analysis is a powerful tool for studying the dynamic changes in Staphylococcus aureus small-colony variants. J Clin Microbiol 44:3274–3278
Beranová J, Jemioła-Rzemińska M, Elhottová D, Strzałka K, Konopásek I (2008) Metabolic control of the membrane fluidity in Bacillus subtilis during cold adaptation. Biochim Biophys Acta 1778:445–453
Bogdanova ES, Bass IA, Minakhin LS, Petrova MA, Mindlin SZ, Volodin AA, Kalyaeva ES, Tiedjet JM, Hobrnan JL, Brown NL, Nikiforov VG (1998) Horizontal spread of mer operons among Gram-positive bacteria in natural environments. Microbiology 144:609–620
Bosch A, Miñán A, Vescina C, Degrossi J, Gatti B, Montanaro P, Messina M, Franco M, Vay C, Schmitt J, Naumann D, Yantorno O (2008) Fourier transform infrared spectroscopy for rapid identification of nonfermenting gram-negative bacteria isolated from sputum samples from cystic fibrosis patients. J Clin Microbiol 46: 2535–2546
Cherry DS, Guthrie RK, Harvey RS (1974) Temperature influence on bacterial populations in three aquatic systems. Water Res 8:149–155
CLSI. Clinical and Laboratory Standards Institute. (2006) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, seventh ed., Approved Standard M7-A7, CLSI,Wayne, PA, USA.
Cossa D, Martin JM, Takayanagi K, Sanjuan J (1997) The distribution and cycling of mercury species in the western Mediterranean. Deep-Sea Res II Top Stud Oceanogr 44:721–740
Das S, Lyla PS, Khan SA (2006) Marine microbial diversity and ecology: importance and future perspectives. Curr Sci 90:1325–1335
Das S, Dash HR, Mangwani N, Chakraborty J, Kumari S (2014) Understanding molecular identification and polyphasic taxonomic approaches for genetic relatedness and phylogenetic relationships of microorganisms. J Microbiol Methods 103:80–100
Dash HR, Das S (2012) Bioremediation of mercury and importance of bacteria mer genes. Int Biodeterior Biodegrad 75:207–213
Dash HR, Das S (2014) Bioremediation potential of mercury by Bacillus species isolated from marine environment and wastes of steel industry. Bioremed J 18:1–9
Dash HR, Das S (2015) Bioremediation of inorganic mercury through volatilization and biosorption by transgenic Bacillus cereus BW-03(pPW-05). Int Biodeterior Biodegrad 103:179–185
Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571
Dash HR, Mangwani N, Das S (2014) Characterization and potential application in mercury bioremediation of highly mercury resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Pollut Res 21:2642–2653
De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10:471–477
De J, Dash HR, Das S (2014) Mercury pollution and bioremediation- a case study on biosorption by a mercury resistant marine bacterium. In: Das S (ed) Microbial Biodegradation and Bioremediation. Elsevier, Waltham, pp 137–167
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Filip Z, Herrmann S, Kubat J (2004) FT-IR spectroscopic characteristics of differently cultivated Bacillus subtilis. Microbiol Res 159:257–262
François F, Lombard C, Guigner JM, Soreau P, Brian-Jaisson F, Martino G, Vandervennet M, Garcia D, Molinier AL, Pignol D, Peduzzi J, Zirah S, Rebuffat S (2012) Isolation and characterization of environmental bacteria capable of extracellular biosorption of mercury. Appl Environ Microbiol 78:1097–1106
Freitas DB, Reis MP, Lima-Bittencourt CI, Costa PS, Assis PS, Chartone-Souza E (2008) Nascimento AMA. Genotypic and phenotypic diversity of Bacillus spp. isolated from steel plant waste, BMC Res Not. doi:10.1186/1756-0500-1-92
Gnanam S, Sivakumar K, Vijayalakshmi S, Balasubramaniyam T (2013) Ambience of physico-chemical characteristics to actinobacterial density in the Chennai coast of the Bay of Bengal, India. Indian J Geo-Mar Sci 42:254–265
Gross L (2007) Untapped bounty: sampling the seas to survey microbial biodiversity. PLoS Biol 5(3), e85. doi:10.1371/journal.pbio.0050085
Gunaseelan C, Ruban P (2011) Heavy metal resistance bacterium isolated from Krishna Godavari basin, Bay of Bengal. Int J Environ Sci 1:1856–1864
Hall BD, Aiken GR, Krabbenhoft DF, Marvin-DiPasquale M, Swarzenski CM (2008) Wetlands as principal zones of methylmercury production in southern Louisiana and the Gulf of Mexico region. Environ Pollut 154:124–134
Hideomi N, Ishikawa T, Yasunaga S, Kondo I, Mitsuhasi S (1977) Frequency of heavy-metal resistance in bacteria from inpatients in Japan. Nature (London) 266:165–167
Hill GT, Mitkowski NA, Aldrich-Wolfe L, Emele LR, Jurkonie DD, Ficke A, Maldonado-Ramireza S, Lynch ST, Nelson EB (2000) Methods for assessing the composition and diversity of soil microbial communities. Appl Soil Ecol 15:25–36
Jaysankar D, Ramaiah N (2006) Occurrence of large fractions of mercury resistant bacteria in the Bay of Bengal. Curr Sci 91:368–372
Kim TG, Yun J, Hong SH, Cho KS (2014) Effects of water temperature and backwashing on bacterial population and community in a biological activated carbon process at a water treatment plant. Appl Microbiol Biotechnol 98:1417–1427
Kostaki M, Chorianopoulos N, Braxou E, Nychas GJ, Giaouris E (2012) Differential biofilm formation and chemical disinfection resistance of sessile cells of Listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Appl Environ Microbiol. doi:10.1128/AEM.07099-11
Kwokal Z, Sarkar SK, Chatterjee M, Franciskovis-Bilinski S, Bilinski H, Bhattacharya A, Bhattacharya BD, Alam MA (2008) An assessment of mercury loading in core sediments of Sunderban Mangrove wetland, India (A preliminary report). Bull Environ Contam Toxicol 81:105–112
Lal D, Lal R (2010) Evolution of mercuric reductase (merA) gene: a case of horizontal gene transfer. Mikrobiologiia 79:524–531
Laurier FJG, Mason RP, Gill GA, Whalin L (2004) Mercury distributions in the North Pacific Ocean: 20 years of observations. Mar Chem 90:3–19
Lin M, Al-Holy M, Al-Qadiri H, Chang S, Kang DH, Rodgers BD, Rasco BA (2007) Phylogenetic and spectroscopic analysis of Alicyclobacillus isolates by 16S rDNA sequencing and mid-infrared spectroscopy. Sens Instrumen Food Qual Saf 1:11–17
MacDonell MT, Singleton FL, Hood MA (1982) Diluent composition for use of API 20E in characterizing marine and estuarine bacteria. Appl Environ Microbiol 44:423–427
Marchand C, Lallier-Verges E, Baltzer F, Alberic P, Cossa D, Baillif P (2006) Heavy metal distribution in mangrove sediments along the mobile coastline of French Guiana. Mar Chem 98:1–17
Martínez-Juárez VM, Cárdenas-González JF, Torre-Bouscoulet ME, Acosta-Rodríguez I (2012) Biosorption of mercury (II) from aqueous solutions onto fungal biomass. Bioinorg Chem Appl. doi:10.1155/2012/156190
Mason RP, Rolfhus KR, Fitzgerald WF (1998) Mercury in the North Atlantic. Mar Chem 61:37–53
Michelim L, Muller G, Zacaria J, Delamare AP, Costa SO, Echeverrigaray S (2008) Comparison of PCR-based molecular markers for the characterization of Proteus mirabilis clinical isolates. Braz J Infect Dis 12:423–429
Mishra RR, Swain MR, Dangar TK, Thatoi HN (2012) Diversity and seasonal fluctuation of predominant microbial communities in Bhitarkanika, a tropical mangrove ecosystem in India. Rev Biol Trop 60:909–924
Morel FM, Kraepiel AM, Amyot M (1998) The chemical cycle and bioaccumulation of mercury. Annu Rev Ecol Evol Syst 29:543–566
Muller KA, Rasmussen LD, Sorensen SJ (2001) Adaptation of the bacteria community to mercury contamination. FEMS Microbiol Lett 204:49–53
Nagvenkar GS, Ramaiah N (2009) Abundance of sewage-pollution indicator and human pathogenic bacteria in a tropical estuarine complex. Environ Monit Assess 155:245–256
Nakamura K, Nakahara H (1988) Simplified X-ray film method for detection of bacterial volatilization of mercury chloride by Escherichia coli. Appl Environ Microbiol 54:2871–2873
Nayak L, Behera DP (2004) Seasonal variation of some physicochemical parameters of the Chilika lagoon (east coast of India) after opening the new mouth, near Sipakuda. Indian J Mar Sci 33:206–208
Nayak BK, Acharya BC, Panda UC, Nayak BB, Acharya SK (2004) Variation of water quality in Chilika lake, Orissa. Indian J Mar Sci 33:164–169
Nesbakken T (2006) Yersinia enterocolitica. In: Motarjemi Y, Adam M (eds) Emerging foodborne pathogens. CRC Press, NewYork, pp 373–406
O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79
Pal C, Palme JB, Rensing C, Kristiansson E, Larsson DGJ (2013) BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res 42:D737–D743
Panda SP, Mishra CSK (2007) Bioremediation of environmental degradation- a feasible option for ecorestoration. In: Mishra CSK, Juwarkar AA (eds) Environmental biotechnology. APH Publishing Corporation. New Delhi, India, pp 153–164
Panda KK, Lenka M, Panda BB (1992) Monitoring and assessment of mercury pollution in the vicinity of a chloralkali plant. III. Concentration and genotoxicity of mercury in the industrial effluent and contaminated water of Rushikulya estuary, India. Mutat Res 280:149–160
APHA (American Public Health Association) (1992) Standard methods for the examination of water and waste water. Wasinghton DC
Raju K, Vijayaraghavan K, Seshachalam S, Muthumanickam J (2011) Impact of anthropogenic input on physicochemical parameters and trace metals in marine surface sediments of Bay of Bengal off Chennai, India. Environ Monit Assess 177:95–114
Ramaiah N, De J (2003) Unusual rise in mercury-resistant bacteria in coastal environments. Microb Ecol 45:444–454
Rasmussen LD, Sørensen SJ (1998) The effect of long term exposure of mercury in the bacterial community in marine sediment. Curr Microbiol 36:291–297
Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30:1148–1160
Rodrigues J, Madhukar A, Kumar N, Sangodkar UMX (2011) Isolation and characterization of a marine bacterium belonging to genus Alkaligens capable of the complete mineralization of the dibenzothiophene. Indian J Geo-Mar Sci 40:391–397
Ruiz ON, Alvarez D, Gonzalez-Ruiz G, Torres C (2011) Characterization of mercury bioremediation by transgenic bacteria expressing metallothionein and polyphosphate kinase. BMC Biotechnol http://www.biomedcentral.com/1472-6750/11/82
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schroeder W, Munthe J (1998) Atmospheric mercury -an overview. Atm Environ 32:809–822
Selvin J, Priya SS, Kiran GS, Thangavelu T, Bai NS (2009) Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiol Res 164:352–363
Sidransky D, Tokino T, Hamilton SR, Kinzler KW, Levin B, Frost P, Vogelstein B (1992) Identification of ras oncogene mutations in the stool of patients with curable colorectal tumors. Science 256:102–105
Sotero-Martins A, Jesus MSD, Lacerda M, Moreira JC, Filgueiras ALL, Barrocas PRG (2008) A conservative region of the mercuric reductase gene (merA) as a molecular marker of bacterial mercury resistance. Braz J Microbiol 39:307–310
Srinivasan V, Natesan U, Parthasarathy A (2013) Seasonal variability of coastal water quality in Bay of Bengal and Palk Strait, Tamilnadu, Southeast coast of India. Braz Arch Biol Technol 56:875–884
Stamper DM, Walch M, Jacobs RN (2003) Bacterial population changes in a membrane bioreactor for gray water treatment monitored by denaturing gradient gel electrophoretic analysis of 16S rRNA gene fragments. Appl Environ Microbiol 69:852–860
Sunderland EM, Mason RP (2007) Human impacts on open ocean mercury concentrations. Glob Biogeochem Cycles 21. doi 10.1029/2006GB002876
Tanaka T, Kuroda M, Sakaguchi K (1977) Isolation and characterization of four plasmids from Bacillus subtilis. J Bacteriol 129:1487–1494
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DJ (1997) CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
U. S. Environmental Protection Agency (1976) National recommended water quality criteria. Washington D. C. 20460
van Dijl JM, Hecker M (2013) Bacillus subtilis: from soil bacterium to super-secreting cell factory. Microb Cell Factories 12 (3)
Venkatesharaju K, Ravikumar P, Somashekhar RK, Prakash KL (2010) Physico-chemical and bacteriological investigation on the river Cauvery of Kollegal stretch in Karnataka. Kathmandu Univ J Sci Eng Technol 6:10–15
von Rozycki T, Nies DH (2009) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 69:115–139
WHO (1993) Guidelines for drinking water quality. Revision of the 1984 guidelines. Final task group meeting. Geneva, 21–25 September 1992
Wieser M, Busse HJ (2000) Rapid identification of Staphylococcus epidermidis. Int J Syst Evol Microbiol 50:1087–1093
Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271
Wommack KE, Ravel J (2013) Microbiome, demystifying the role of microbial communities in the biosphere. Microbiome 1 (1)
Zhang W, Chen L, Liu D (2012) Characterization of a marine-isolated mercury-resistant Pseudomonas putida strain SP1 and its potential application in marine mercury reduction. Appl Microbiol Biotechnol 93:1305–1314
Zhang W, Yin K, Li B, Chen L (2013) A glutathione S-transferase from Proteus mirabilis involved in heavy metal resistance and its potential application in removal of Hg2+. J Hazard Mater 261:646–652
Acknowledgments
Authors would like to acknowledge the authorities of NIT, Rourkela for providing facilities. H.R.D. gratefully acknowledges the receipt of research fellowship from Ministry of Human Resource Development, Government of India. S.D. thanks the Department of Biotechnology, Government of India for research grants on marine bacterial biofilm based enhanced bioremediation of PAHs and heavy metals.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Robert Duran
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 856 kb)
Rights and permissions
About this article
Cite this article
Dash, H.R., Das, S. Diversity, community structure, and bioremediation potential of mercury-resistant marine bacteria of estuarine and coastal environments of Odisha, India. Environ Sci Pollut Res 23, 6960–6971 (2016). https://doi.org/10.1007/s11356-015-5991-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-5991-4