Abstract
Heavy metals influence the population size, diversity, and metabolic activity of bacteria. In turn, bacteria can develop heavy metal resistance mechanisms, and this can be used in bioremediation of contaminated areas. The purpose of the present study was to understand how heavy metals concentration influence on diversity and distribution of heavy metal-resistant bacteria in Araça Bay, São Sebastião, on the São Paulo coast of Brazil. The hypothesis is that activities that contribute for heavy metal disposal and the increase of metals concentrations in environment can influence in density, diversity, and distribution of heavy metal-resistant bacteria. Only 12 % of the isolated bacteria were sensitive to all of the metals tested. We observed that the highest percentage of resistant strains were in areas closest to the São Sebastião channel, where port activity occurs and have bigger heavy metals concentrations. Bacterial isolated were most resistant to Cr, followed by Zn, Cd, and Cu. Few strains resisted to Cd levels greater than 200 mg L−1. In respect to Cr, 36 % of the strains were able to grow in the presence of as much as 3200 mg L−1. Few strains were able to grow at concentrations of Zn and Cu as high as 1600 mg L−1, and none grew at the highest concentration of 3200 mg L−1. Bacillus sp. was most frequently isolated and may be the dominant genus in heavy metal-polluted areas. Staphylococcus sp., Planococcus maritimus, and Vibrio aginolyticus were also isolated, suggesting their potential in bioremediation of contaminated sites.
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Sun W, Zhou Q, Xie X, Liu R (2010) Spatial, sources and risk assessment of heavy metal contamination of urban soils in typical regions of Shenyang, China. J Hazard Mat 174:455–462. doi:10.1016/j.jhazmat.2009.09.074
Andrade S, Poblet A, Scagliola M, Vodopivez C, Curtosi A, Pucci A, Marcovecchio J (2001) Distribution of heavy metals in surface sediments from an Antarctic marine ecosystem. Environ Monit Assess 66:147–158
Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69:2313–2320
Hortellani MA, Sarkis JES, Abessa DMS, Sousa ECPM (2008) Avaliação da contaminação por elementos metálicos dos sedimentos do estuário Santos–São Vicente. Química Nov. 31:10–19. doi:10.1590/S0100-40422008000100003
Yang H, Rose NL (2003) Distribution of Hg in six lake sediments core across the UK. Sci Total Environ 304:391–404. doi:10.1016/S0048-9697(02)00584-3
Pinto AB, Pagnocca FC, Pinheiro MA, Fontes RF, Oliveira AJ (2015) Heavy metals and TPH effects on microbial abundance and diversity in two estuarine areas of the Southern-central coast of São Paulo State, Brazil. Mar Pollut Bull 96:410–417. doi:10.1016/j.marpolbul.2015.04.014
Poole RK, Gadd GM (1989) Metals: microbe interactions. IRL Press, Oxford, pp 1–37
Ji G, Silver S (1995) Bacterial resistance mechanism for heavy metals of environmental concern. J Indust Microbiol 14:61–75
Wang Y, Shi J, Wang H, Chen OL, Chen Y (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotox Environ Safat 67:75–81. doi:10.1016/j.ecoenv.2006.03.007
Oliveira A, Pampulha ME (2006) Effects of long-term heavy metal contamination on soil microbial characteristics. J Biosci Bioeng 102:157–161. doi:10.1263/jbb.102.157
Giller PS, Malmqvist B (1998) The biology of streams and rivers. Oxford University Press, New York
Matyar F (2012) Antibiotic and heavy metal resistance in bacteria isolated from the Eastern Mediterranean Sea coast. Bull Environ Contam Toxicol 89:551–556. doi:10.1007/s00128-012-0726-4
Glöckner FO, Stal LJ, Sandaa RA, Gasol JM, O’Gara F, Hernandez F, Labrenz M, Stoica E, Varela MM, Bordalo A, Pitta P (2012) Marine microbial diversity and its role in ecosystem functioning and environmental change. In: Calewaert JB, McDonough N (eds) Marine Board Position Paper 17. Marine Board-ESF, Ostend, Belgium
Gillan DC, Danis B, Pernet P, Joly G, Dubois P (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Environ Microbiol 71:679–690
Banerjee S, Gothalwal R, Sahu PK, Sao S (2015) Microbial observation in bioaccumulation of heavy metals from the ash dyke of thermal power plants of Chhattisgarh, India. Adv Biosc Biotechnol 6:131–138. doi:10.4236/abb.2015.62013
Outten FW, Outten CE, O’halloran T (2000) Metalloregulatory systems at the interface between bacterial metal homeostasis and resistance. In: Storz G, Hengge-Aronis RR (eds) Bacterial stress responses. ASM Press, Washington, D.C, pp 145–157
Hasin AA, Gurman SJ, Murphy LM, Perry A, Smith TJ, Gardiner PE (2010) Remediation of chromium(VI) by a methane-oxidizing bacterium. Environ Sci Technol 44:400–405. doi:10.1021/es901723c
Dash HR, Magdwani N, Chakraboryi J, Kumari S, Das S (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571. doi:10.1007/s00253-012-4584-0
Kacar A, Kocyigit A (2013) Characterization of heavy metal and antibiotic resistant bacteria isolated from Aliaga Ship Dismantling Zone, Eastern Aegean Sea, Turkey. Int J Environ Res 7:895–902
Nithia C, Pandian SK (2010) Isolation of heterotrophic bacteria from Palk Bay sediments showing heavy metal tolerance and antibiotic production. Microbiol Res 165:578–593. doi:10.1016/j.micres.2009.10.004
ANTAQ. Porto de São Sebastião. Available in: www.antaq.gov.br/portal/pdf/portos/2012/saosebastiao.pdf; Accessed in: 05/09/2015.
Amaral ACZ, Migotto AE, Turra A, Svhaeffer-Novelly Y (2010) Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10:1–47. doi:10.1590/S1676-06032010000100022
Gubitoso S (2010) Influência de efluentes domésticos e petroquímicos em sedimentos e carapaças de foraminíferos do canal de São Sebastião, SP. Dissertação (Mestrado) – Instituto de Geociências, Universidade de São Paulo, São Paulo
Feng H, Han X, Zhang W, Yu L (2004) A preliminary study of heavy metal contamination in Yangtze River Interdital zone due to urbanization. Mar Poll Bull 49:910–915. doi:10.1016/j.marpolbul.2004.06.014
Akinbowale OL, Peng H, Grant P, Barton MD (2007) Antibiotic and heavy metal resistance in motile aeromonads and pesudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Agents 30:177–182
Ansari MI, Malik A (2007) Biosorption of nickel and cadmium by metal resistant bacterial isolates from agricultural soil irrigated with industrial wastewater. Bioresour Techno 98:3149–3153
Embley TM, Stackebrandt E (1994) The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 48:257–289
Sievers F, Wilm A, Dineen D, Gibson TJ, KarplusK LW, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. doi:10.1038/msb.2011.75
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197
Abessa DMS, Carr RS, Rachid BRF, Sousa ECPM, Hortelani MA, Sarkis JE (2005) Influence of a Brazilian sewage outfall on the toxicity and contamination of adjacent sediments. Mar Pollut Bull 50:875–885
USEPA (United States Environmental Protection Agency) (1994) Method 3051. Microwave assisted cid digestion of sediments, sludges. Soils and oilsl. Revision 0. September.
CCME (2002) Canadian environmental quality guidelines, National Guidelines and Standards Office. Canadian Council of Ministers of the Environment, Winnipeg, p 12
Föstner UG, Wittmann GTW (1981) Metal pollution in the aquatic environmental. Springer-Verlag, Berlin
Abessa DM, Rachid BR, Moser GA, Oliveira AJF (2012) Efeitos ambientais da disposição oceânica de esgotos por meio de emissários submarinos: uma revisão. O Mundo da Saúde 36:643–661
Castro-Filho BM (1990) Wind driven currents in the Channel of São Sebastião: winter, 1979. Boletim do Instituto Oceanográfico 38:111–132
Fontes RFC (1995) As Correntes no Canal de São Sebastião. Dissertação de Mestrado. IOUSP, 159p
Azam F, Vaccaro RF, Gillespie PA, Moussalli EI, Hodson RE (1977) Controlled ecosystem pollution experiment: effect of mercury on enclosed water columns. Mar bacterioplank Mar Sci Comm 3:313–329
Malik A, Khan IF, Aleem A (2002) Plasmid incidence in bacteria from agricultural and industrial soils. World J Microbiol Biotechnol 18:827–833
Torsvik V, Sørheim R, Goksøyr J (1996) Total bacterial diversity in soil and sediment communities—a review. J Indust Microbiol 17:170–178
Arslam P, Beltrame M, Tomasi A (1987) Intracelullar chromium reduction. Bioch Biphys Acta 931:10–15
Choudhury R, Srivastava S (2001) Zinc resistance mechanisms in bacteria. Current Sci 81:768–775
Duxbury T (1981) Toxicity of heavy metals to soil bacteria. FEMS Microbiol Letters 11:217–220
Achard-Joris M, Moreau JL, Lucas M, Baudrimont M, Mesmer-Dudons N, Gonsalez P, Boudou A, Bordineaud JP (2007) Role of metallothioneins in superoxide radical generation during copper redox cycling: defining the fundamental function of metallothioneins. Biochemie 9:1474–1488. doi:10.1016/j.biochi.2007.06.005
Duxbury T, Bicknell B (1983) Metal tolerant bacterial population populations from natural and metal polluted soils. Soil Biol Bioch 15:243–250
Kafilzadeh F, Zahirian Y, Zolgharnein H (2013) Isolation and molecular identification of mercury resistant bacteria and detection of Escherichia coli mercuric reductase gene from wastewater of Khowr-e-Musa, Iran. Int J Biosc 3:313–318. doi:10.12692/ijb/3.8.313-318
Matyar F, Kaya A, Dinçer S (2008) Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Sci Total Environ 407:279–285. doi:10.1016/j.scitotenv.2008.08.014
Malik A, Jaiswal R (2000) Metal resistance in Pseudomonas strains isolated from soil treated with industrial wastewater. World J Microbiol Biotechnol 16:177–182
Spain A, Alm C (2003) Implications of microbial heavy metal tolerance in the environment. Rev Undergrad Res 2:1–6
Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of Gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73:3272–3282
Zobeel CE (1946) Marine microbiology: a monograph on hydrobacteriology. Chronica Botanica Co, Walthman, M.A
Stach JEM, Bull AT (2005) Estimating and comparing the diversity of marine actinobacteria. Antonie Leeuwenhoek 87:3–9
Jensen PR, Mincer J, Williams PG, Fenical W (2005) Marine actinomycete diversity and natural product discovery. Antonie Leeuwenhoek 87:43–48
Belliveau BH, Staradub ME, Trevor JT (1991) Occurrence of antibiotic and metal resistance and plasmids in Bacillus strains isolated from marine sediment. Canad J Microbiol 37:513–520
Kamala-Kannan S, Mahadevan S, Krishnamoorthy R (2006) Characterization of a mercury-reduncing Bacillus cereus isolated from the Publicat Lake sediments, South East Coast of India. Archiv Microbiol 185:202–211
Kamala-Kannan S, Krishnamoorthy R, Lee KJ, Purosothaman A, Santhi K, Rao NR (2007) Aerobic chromate reduncing Bacillus cereus isolated from the heavy metal contaminated ennore creek sediment, North of Chennai, Tamil Nadu, South East. India Res J Microbiol 2:133–140
Kamala-Kannan S, Lee KJ (2008) Metal tolerance and antibiotic resistance of Bacillus species isolated from Sunchon Bay, South Korea. Biotechnol 7:149–152
Baker-Austin C, Wright MS, Stepaunauskas R, Mcarthur JV (2006) Co-selection of antibiotic and heavy metal resistance. Trends Microbiol 14:176–182. doi:10.3389/fmicb.2012.00399
SCENIHR. Scientific Committee on Emerging and Newly Identified Health Risks (2009) Assessment of the antibiotic resistance effects of biocides http://ec.europa.eu/health/ph_risk/committees/04_scenihr/docs/scenihr_o_021.pdf, Accessed in: 27 de setembro de 2014.
Hasman H, Aarestrup FM (2002) tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptides resistance. Antib Agents Chemot 46:1410–1416
Martínez JL (2011) Bottlenecks in the transferability of antibiotic resistance from natural ecosystems to human bacterial pathogens. Front Microbio 2:265. doi:10.3389/fmicb.2011.00265
Velázquez-Meza ME (2005) Staphylococcus aureus methicillin-resistant: emergence and dissemination. Salud Publica Mex 47:381–387
Anderson Borge GI, Skeie M, Sorhaug T, Langsrud T, Granum PE (2001) Growth and toxin profiles of Bacillus cereus isolated from different food sources. Int J Food Microbiol 69:237–246
Acknowledgments
The authors would like to thank UNESP and all members of the Marine Microbiology Laboratory (MICROMAR) and of the Structural Molecular Biology Laboratory (LABIMES). The Brazilian agency known as the Coordination for the Improvement of Higher Education Personnel (CAPES) and São Paulo Research Foundation (FAPESP) are acknowledged for financial support: The Biota Araça Research Project (process number: 2011/50317-5), coordinated by Dr. Cecília Amaral.
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Zampieri, B.D.B., Pinto, A.B., Schultz, L. et al. Diversity and Distribution of Heavy Metal-Resistant Bacteria in Polluted Sediments of the Araça Bay, São Sebastião (SP), and the Relationship Between Heavy Metals and Organic Matter Concentrations. Microb Ecol 72, 582–594 (2016). https://doi.org/10.1007/s00248-016-0821-x
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DOI: https://doi.org/10.1007/s00248-016-0821-x