Abstract
Environmental health is a critical concern, continuously contaminated by physical and biological components (viz., anthropogenic activity), which adversely affect on biodiversity, ecosystems and human health. Nonetheless, environmental pollution has great impact on microbial communities, especially bacteria, which try to evolve in changing environment. For instance, during the course of adaptation, bacteria easily become resistance to antibiotics and heavy metals. Antibiotic resistance genes are now one of the most vital pollutants, provided as a source of frequent horizontal gene transfer. In this review, the environmental cause of multidrug resistance (MDR) that was supposed to be driven by either heavy metals or combination of environmental factors was essentially reviewed, especially focussed on the correlation between accumulation of heavy metals and development of MDR by bacteria. This kind of correlation was seemed to be non-significant, i.e. paradoxical. Gram-positive bacteria accumulating much of toxic heavy metal (i.e. highly stress tolerance) were unlikely to become MDR, whereas Gram-negative bacteria that often avoid accumulation of toxic heavy metal by efflux pump systems were come out to be more prone to MDR. So far, other than antibiotic contaminant, no such available data strongly support the direct influence of heavy metals in bacterial evolution of MDR; combinations of factors may drive the evolution of antibiotic resistance. Therefore, Gram-positive bacteria are most likely to be an efficient member in treatment of industrial waste water, especially in the removal of heavy metals, perhaps inducing the less chance of antibiotic resistance pollution in the environment.
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References
Abraham EP, Chain E (1940) An enzyme from bacteria able to destroy penicillin. Nature 146:837
Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation, a review. IIOABJ 3:39–46
Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98:2243–2257
Ahmed S, Siddique MA, Rahman M, Bari ML, Ferdousi S (2019) A study on the prevalence of heavy metals, pesticides, and microbial contaminants and antibiotics resistance pathogens in raw salad vegetables sold in Dhaka, Bangladesh. Heliyon 5:e01205
Akmal M, Wang HZ, Wu JJ (2005) Changes in enzymes activity, substrate utilization pattern and diversity of soil microbial communities under cadmium pollution. J Environ Sci 17:802–807
Alonso A, Sánchez P, Martínez JL (2001) Environmental selection of antibiotic resistance genes. Environ Microbiol 3:1–9
Baquero F, Martinez JL, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265
Barber M (1947) Staphylococcal infection due to penicillin-resistant strains. BMJ 2:863–865
Barber M, Rozwadowska-Dowzenko M (1948) Infection by penicillin-resistant staphylococci. Lancet 2:641–642
Bass L, Liebert CA, Lee MD, Summers AO, White DG, Thayer SG, Maurer JJ (1999) Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli. Antimicrob Agents Chemother 43:2925–2929
Bednorz C, Oelgeschläger K, Kinnemann B, Hartmann S, Neumann K, Pieper R et al (2013) The broader context of antibiotic resistance: zinc feed supplementation of piglets increases the proportion of multi-resistant Escherichia coli in vivo. Int J Med Microbiol 303:396–403
Beveridge TJ, Murray RGE (1980) Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol 141:876–887
Bhullar K, Waglechner N, Pawlowski A, Koteva K, Banks ED, Johnston MD, Barton HA, Wright GD (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE 7:e34953
Boy-Roura M, Mas-Pla J, Petrovic M, Gros M, Soler D, Brusi D, Menció A (2018) Towards the understanding of antibiotic occurrence and transport in groundwater: findings from the Baix Fluvià alluvial aquifer (NE Catalonia, Spain). Sci Total Environ 612:1387–1406
Bush K, Courvalin P, Dantas G, Davies J, Eisenstein B et al (2011) Tackling antibiotic resistance. Nat Rev Microbiol 9:894–896
Cavicchioli R, Thomas T (2002) Extremophiles. Encyclopedia of microbiology, vol 2. Academic Press, San Diego, pp 317–337
Centers for Disease Control and Prevention (2013) Antibiotic resistance threats in the United States. Centers for Disease Control and Prevention, Atlanta
Chihomvu P, Stegmann P, Pillay M (2015) Characterization and Structure Prediction of Partial Length Protein Sequences of pcoA, pcoR and chrB Genes from Heavy Metal Resistant Bacteria from the Klip River, South Africa. Int J Mol Sci 16:7352–7374
Conejo MC, García I, Martínez LM, Picabea L, Pascual A (2003) Zinc eluted from siliconized latex urinary catheters decreases OprD expression, causing carbapenem resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47:2313–2315
Cycoń M, Mrozik A, Piotrowska-Seget Z (2019) Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity. Front Microbiol 10:338
D’Costa VM, Osta VM, King CE, Kalan L, Morar M, Sung WWL et al (2011) Antibiotic resistance is ancient. Nature 477:457–461
Davies SC, Fowler T, Watson J, Livermore DM, Walker D (2013) Annual report of the chief medical officer: infection and the rise of antimicrobial resistance. Lancet 381:1606–1609
Delcour AH (2009) Outer membrane permeability and antibiotic resistance. Biochim Biophys Acta Proteins Proteom 1794:808–816
Diorio C, Cai J, Marmor J, Shinder R, DuBow MS (1995) An Escherichia coli chromosomal ars operon homolog is functional in arsenic detoxification and is conserved in gram-negative bacteria. J Bacteriol 177:2050–2056
Dixit R (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7:2189–2212
Doyle RJ, Matthews TH, Streips UN (1980) Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall. J Bacteriol 143:471–480
Drury B, Scott J, Rosi-Marshall EJ, Kelly JJ (2013) Triclosan exposure increases triclosan resistance and influences taxonomic composition of benthic bacterial communities. Environ Sci Technol 47:8923–8930
Dua M, Singh A, Sethunathan N, Johri A (2002) Biotechnology and bioremediation: successes and limitations. Appl Microbiol Biotechnol 59:143–152
Eichner CA, Erb RW, Timmis KN, Wagner-Dobler I (1999) Thermal gradient gel electrophoresis analysis of bioprotection from pollutant shocks in the activated sludge microbial community. Appl Environ Microb 65:102–109
Ellis RJ, Morgan P, Weightman AJ, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl Environ Microbiol 69:3223–3230
Elsgaard L, Petersen SO, Debosz K (2001) Effects and risk assessment of linear alkylbenzene sulfonates in agricultural soil: 1. Short-term effects on soil microbiology. Environ Toxicol Chem 20:l656-1663
European Centre for Disease Prevention and Control Joint Report with EMEA (2011) The bacterial challange: time to react. https://ecdc.europa.eu/en/publications-data/ecdcemea-joint-technical-report-bacterial-challenge-time-react. Accessed on 5 Jan 2019
Figueiredo R, Card RM, Nunez-Garcia J, Mendonc N, Jorge da Silva G, Anjum MF (2018) Multidrug-resistant Salmonella enterica isolated from food animal and foodstuff may also be less susceptible to heavy metals. Foodborne Pathog Dis 16:166–172
Finland M (1979) Emergence of antibiotic resistance in hospitals, 1935–1975. Rev Infect Dis 1:4–22
Finley RL, Collignon P, Larsson DGJ, McEwen SA, Li XZ, Gaze WH et al (2013) The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 57:704–710
Fleming A (1929) On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. Bri J Exp Pathol 10:226
Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617
Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60
Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390
Gaynes R (2017) The discovery of penicillin—new insights after more than 75 years of clinical use. Emerg Infect Dis 23:849
Gaze WH, Abdouslam N, Hawkey PM, Wellington EMH (2005) Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob Agents Chemother 49:1802–1807
Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D, Andersson DI (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7:e1002158
Hasman H, Aarestrup FM (2005) Relationship between copper, glycopeptide, and macrolide resistance among Enterococcus faecium strains isolated from pigs in Denmark between 1997 and 2003. Antimicrob Agents Chemother 49:454–456
Hawkey PM (2015) Multidrug-resistant gram-negative bacteria: a product of globalization. J Hosp Infect 89:241–247
Hayashi S, Abe M, Kimoto M, Furukawa S, Nakazawa T (2000) The DsbA–DsbB disulfide bond formation system of Burkholderia cepacia is involved in the production of protease and alkaline phosphatase, motility, metal resistance, and multi-drug resistance. Microbiol Immunol 44:41–50
Henriksson PJG, Rico A, Troell M, Klinger DH, Buschmann AH, Saksida S, Chadag MV, Zhang W (2018) Unpacking factors influencing antimicrobial use in global aquaculture and their implication for management: a review from a systems perspective. Sustain Sci 13:1105–1120
Henriques I, Marta T, Leite L, Fidalgo C, Araújo S, Oliveira C, Alves A (2016) Co-selection of antibiotic and metal(loid) resistance in gram-negative epiphytic bacteria from contaminated salt marshes. Mar Pollut Bull 109:427–434
Hrynkiewicz K, Baum C (2014) Application of microorganisms in bioremediation of environment from heavy metals. Environmental deterioration and human health book. Springer, Berlin, pp 215–227
Hussein H, Ibrahim SF, Kandeel K, Moawa H (2004) Biosorption of heavy metals from waste water using Pseudomonas sp. Electronic J Biotechnol 7:1
Ivshina IB, Kostina LV, Kamenskikh TN, Zhuikova VA, Zhuikova TV, Bezel VS (2014) Soil microbiocenosis as an indicator of stability of meadow communities in the environment polluted with heavy metals. Russ J Ecol 45:83–89
Jasmine R, Venkadesan B, Ragul K (2012) Identification and characterization of heavy metal-resistant Pseudomonas aeruginosa and its potential for bioremediation. Am J Pharm Tech Res 2:783–787
Ji G, Silver S (1992) Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J Bacteriol 174:3684–3694
Jović M, Onjia A, Stanković S (2012) Toxic metal health risk by mussel consumption. Environ Chem Lett 10:69–77
Kang SY, Lee JU, Kim KW (2007) Biosorption of Cr (III) and Cr (VI) onto the cell surface of Pseudomonas aeruginosa. Biochem Eng J 36:54–58
Kang S, Nostrand JDV, Gough HL, He Z, Hazen TC, Stahl DA, Zhou J (2013) Functional gene array-based analysis of microbial communities in heavy metals-contaminated lake sediments. FEMS Microbiol Ecol 86:200–214
Kim S, Lieberman TD, Kishony R (2014) Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance. Proc Natl Acad Sci USA 111:14494–14499
Knapp CW, Dolfing J, Ehlert PAI, Graham DW (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44:580–587
Kuan WH, Hu CY, Chiang MC (2009) Treatment of As (V) and As (III) by electrocoagulation using Al and Fe electrode. Water Sci Technol 60:1341–1346
Kunito T, Oyaizu H, Matsumoto S (1998) Ecology of soil heavy metal-resistant bacteria and perspective of bioremediation of heavy metal-contaminated soils. Rec Res Dev Agric Biol Chem 2:185–206
Learman DR, Ahmad Z, Brookshier A, Henson MW, Hewitt V, Lis A et al (2019) Comparative genomics of 16 Microbacterium spp that tolerate multiple heavy metals and antibiotics. PeerJ 6:e6258
Lee LJ, Barrett JA, Poole RK (2005) Genome wide transcriptional response of chemostat-cultured Escherichia coli to zinc. J Bacteriol 187:1124–1134
Letters RB (2011) Isolation of heavy metal resistant bacterial strains from the battery manufactured polluted environment. Rom Biotechnol Lett 16:102–106
Li J, Richter DD, Mendoza A, Heine P (2008) Four-decade responses of soil trace elements to an aggrading old-field forest: B, Mn, Zn, Cu, and Fe. Ecology 89:2911–2923
Livermore DM (2011) Discovery research: the scientific challenge of finding new antibiotics. J Antimicrob Chemother 66:1941–1944
Mauldin PD, Salgado CD, Hansen IS, Durup DT, Bosso JA (2010) Attributable hospital cost and length of stay associated with health care-associated infections caused by antibiotic-resistant gram-negative bacteria. Antimicrob Agents Chemother 54:109–115
Monachese M, Burton JP, Reid G (2012) Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics. Appl Environ Microbiol 78:6397–6404
Mouedhen G, Feki M, De Petris-Wery M, Ayedi HF (2009) Electrochemical removal of Cr (VI) from aqueous media using iron and aluminum as electrode materials, towards a better understanding of the involved phenomena. J Hazard Mater 168(2–3):983–991
Naguib MM, Khairalla AS, El-Gendy AO, Elkhatib WF (2019) Isolation and characterization of mercury-resistant bacteria from wastewater sources in Egypt. Can J Microbiol 65:308–321
Nanda M, Kumar V, Sharma DK (2019) Multimetal tolerance mechanisms in bacteria: the resistance strategies acquired by bacteria that can be exploited to ‘clean-up’ heavy metal contaminants from water. Aquat Toxicol 212:1–10
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Nelson RE, Slayton RB, Stevens VW, Jones MM, Khader K, Rubin MA et al (2017) Attributable mortality of healthcare-associated infections due to multidrug resistant gram-negative bacteria and methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol 38:848–856
Nies DH (1995) The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J Bacteriol 177:2707–2712
Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biot 51:730–750
Nowicki EM, O’Brien JP, Brodbelt JS, Trent MS (2015) Extracellular zinc induces phosphoethanolamine addition to Pseudomonas aeruginosa lipid A via the ColRS two-component system. Mol Microbiol 97:166–178
Perron K, Caille O, Rossier C, Van Delden C, Dumas JL, Köhler T (2004) CzcR–CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J Biol Chem 279:8761–8768
Perron GG, Whyte L, Turnbaugh PJ, Goordial J, Hanage WP, Dantas G, Desai MM (2015) Functional characterization of bacteria isolated from ancient arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLoS ONE 10:e0069533
Polti MA, Amoroso M, Abate C (2007) Chromium (VI) resistance and removal by actinomycete strains isolated from sediments. Chemosphere 67:660–667
Rahim M, Ullah I, Khan A, Haris MRHM (2016) Health risk from heavy metals via consumption of food crops in the vicinity of District Shangla. J Chem Soc Pak 38:177–185
Rahman Z, Singh VP (2014) Cr(VI) reduction by Enterobacter sp DU17 isolated from the tannery waste dump site and characterization of the bacterium and the Cr(VI) reductase. Int Biodeterior Biodegrad 91:97–103
Rajendran P, Muthukrishnan J, Gunasekaran P (2003) Microbes in heavy metal remediation. Indian J Exp Biol 41:935–944
Ramírez R (2013) The gastropod Osilinus atrataas a bioindicator of Cd, Cu, Pb and Zn contamination in the coastal waters of the Canary Islands. Chem Ecol 29:208–220
Rani A, Goel R (2009) Strategies for crop improvement in contaminated soils using metal-tolerant bioinoculants. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer, Berlin, pp 105–132
Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360
Röling WFM, Van Verseveld HW (2002) Natural attenuation: what does the subsurface have in store? Biodegradation 13:53–64
Rossolini GM, Arena F, Pecile P, Pollini S (2014) Update on the antibiotic resistance crisis. Curr Opin Pharmacol 18:56–60
Ruppe E, Woerther PL, Barbier F (2015) Mechanisms of antimicrobial resistance in Gram-negative bacilli. Ann Intensive Care 5:61
Sandaa RA, Torsvik V, Enger O (2001) Influence of long-term heavy metal contamination on microbial communities in soil. Soil Biol Biochem 33:287–295
Schlesinger WH, Cole JJ, Finzi AC, Holland EA (2011) Introduction to coupled biogeochemical cycles. Front Ecol Environ 9:5–8
Sharma S (2012) Bioremediation: features, strategies and applications. Asian J Pharm Sci 2:202–213
Smith JM, Feil EJ, Smith NH (2000) Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22:1115–1122
Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, McArthur JV (2005) Elevated microbial tolerance to metals and antibiotics in metal-contaminated industrial environments. Environ Sci Technol 39:3671–3678
Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV (2006) Co-selection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8:1510–1514
Summers AO (2002) Generally overlooked fundamentals of bacterial genetics and ecology. Clin Infect Dis 34:S85–S92
Summers AO, Wireman J, Vimy MJ, Lorscheider FL, Marshall B, Levy SB, Bennett S, Billard L (1993) Mercury released from dental silver fillings provokes an increase in mercury-resistant and antibiotic resistant bacteria in oral and intestinal floras of primates. Antimicrob Agents Chemother 37:825–834
Tacão M, Correia A, Henriques I (2012) Resistance to broad spectrum antibiotics in aquatic systems: anthropogenic activities modulate the dissemination of bla(CTX-M)-like genes. Appl Environ Microbiol 78:4134–4140
Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microb 56:782–787
Türkmen M, Türkmen A, Tepe Y, Töre Y, Ateş A (2009) Determination of metals in fish species from Aegean and Mediterranean seas. Food Chem 113:233–237
Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 112:5649–5654
Veglio F, Beolchini F, Gasbarro A (1997) Biosorption of toxic heavy metals, an equilibrium study using free cells of Arthrobacter sp. Process Biochem 32:99–105
Verma N, Singh M (2005) Biosensors for heavy metals. Biometals 18:121–129
Viti C, Pace A, Giovannetti L (2003) Characterization of Cr(VI) resistant bacteria isolated from chromium contaminated soil by tannery activity. Curr Microbiol 46:1–5
Volesky B (1990) Biosorption and biosorbents. Biosorption of heavy metals. CRC Press, Florida, pp 3–44
Waldron PJ, Wu L, Van Nostrand JD, Schadt CW, He Z, Watson DB, Jardine PM et al (2009) Functional gene array-based analysis of microbial community structure in groundwaters with a gradient of contaminant levels. Environ Sci Technol 43:3529–3534
Wieczorek-Dąbrowska M, Tomza-Marciniak A, Pilarczyk B, Balicka-Ramisz A (2013) Roe and red deer as bioindicators of heavy metals contamination in north-western Poland. Chem Ecol 29:100–110
Wireman J, Liebert CA, Smith T, Summers AO (1997) Association of mercury resistance with antibiotic resistance in the Gram-negative fecal bacteria of primates. Appl Environ Microbiol 63:4494–4503
Younessi N, Safari Sinegani AA, Khodakaramian GH (2019) Detection of antibiotic resistance genes in culturable bacteria isolated from soils around mines in Hamedan. Iran Int J Environ Sci Technol 16:7643–7652
Zeeshanur R, Thomas L, Singh V (2019) Biosorption of heavy metals by a lead (Pb) resistant bacterium, Staphylococcus hominis strain AMB-2. J Basic Microbiol 59:477–486
Zhou J (2003) Microarrays for bacterial detection and microbial community analysis. Curr Opin Microbiol 6:288–294
Zhou J, Xia B, Treves DS, Wu LY, Marsh TL, O’Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microb 68:326–334
Zhu J, Zhanga J, Li Q, Hana T, Xieab J, Huab Y, Chaibc L (2013) Phylogenetic analysis of bacterial community composition in sediment contaminated with multiple heavy metals from the Xiangjiang River in China. Mar Pollut Bull 70:134–139
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RB 1 is thankful to the Principal, Symsundar College, Shymsundar, Burdwan for conducting the research. Authors are also thankful to UGC-Center of Advanced Study and DST-FIST, Department of Botany, The University of Burdwan for pursuing research activities. U.H. is thankful to SRF (state-funded) for the finance assistance [Fc (Sc.)/RS/SF/BOT./2017-18/22]. A.K. is thankful to DHESTBT (WB-DBT) for providing the research fund [Memo no. 30 (Sanc.)-BT/ST/P/S&T/2G-48/2017].
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Biswas, R., Halder, U., Kabiraj, A. et al. Overview on the role of heavy metals tolerance on developing antibiotic resistance in both Gram-negative and Gram-positive bacteria. Arch Microbiol 203, 2761–2770 (2021). https://doi.org/10.1007/s00203-021-02275-w
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DOI: https://doi.org/10.1007/s00203-021-02275-w