antibiotics and antibiotic resistance in water environments

Available online at www.sciencedirect.com

Antibiotics and antibiotic resistance in water environmentsFernando Baquero1,3, Jose-Luis Martınez2,3 and Rafael Canton1,3

Antibiotic-resistant organisms enter into water environments

from human and animal sources. These bacteria are able to

spread their genes into water-indigenous microbes, which also

contain resistance genes. On the contrary, many antibiotics

from industrial origin circulate in water environments,

potentially altering microbial ecosystems. Risk assessment

protocols for antibiotics and resistant bacteria in water, based

on better systems for antibiotics detection and antibiotic-

resistance microbial source tracking, are starting to be

discussed. Methods to reduce resistant bacterial load in

wastewaters, and the amount of antimicrobial agents, in most

cases originated in hospitals and farms, include optimization of

disinfection procedures and management of wastewater and

manure. A policy for preventing mixing human-originated and

animal-originated bacteria with environmental organisms

seems advisable.

Addresses1 Department of Microbiology, Ramon y Cajal University Hospital,

CIBER-ESP, Spain2 National Center for Biotechnology, CSIC, Spain3 Joint Unit for Antimicrobial Resistance and Virulence, 28034 Madrid,

Spain

Corresponding author: Baquero, Fernando ([email protected])

Current Opinion in Biotechnology 2008, 19:260–265

This review comes from a themed issue on

Environmental Biotechnology

Edited by Carla Pruzzo and Pietro Canepari

Available online 4th June 2008

0958-1669/$ – see front matter

# 2008 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.copbio.2008.05.006

IntroductionHuman and animal pathogenic and potentially patho-

genic bacteria are constantly released with wastewater

into the water environment. Many of these organisms

harbor antibiotic-resistance genes, eventually inserted

into genetic mobile platforms (plasmids, transposons,

integrons) able to spread among water and soil bacterial

communities [1]. Water constitutes not only a way of

dissemination of antibiotic-resistant organisms among

human and animal populations, as drinking water is

produced from surface water, but also the route by which

resistance genes are introduced in natural bacterial eco-

systems. In such systems, nonpathogenic bacteria could

serve as a reservoir of resistance genes and platforms.

Moreover, the introduction (and progressive accumu-


lation) in the environment of antimicrobial agents, deter-

gents, disinfectants, and residues from industrial

pollution, as heavy metals, contributes to the evolution

and spread of such resistant organisms in the water

environment. The heavy use of prophylactic antibiotics

in aquaculture [2] can be particularly relevant. On the

contrary, environmental bacteria act as an unlimited

source of genes that might act as resistance genes when

entering in pathogenic organisms. Note that many of

these genes are not primarily resistance genes, but belong

to the hidden ‘resistome’ [3], the set of genes able to be

converted in antibiotic-resistance genes. Human health

risk assessment protocols for antibiotic and resistant bac-

teria in water are starting to be discussed [4]. Certainly it

is difficult to believe why public health officers and eco-

toxicologists have failed for more than a century to

seriously propose the absolute need of preventing the

mix between microorganisms from human–animal and

environmental compartments.

The four genetic reactors in antibioticresistanceAntibiotic resistance evolves in bacteria because of the

effect of industrially produced antimicrobial agents on

bacterial populations and communities. Genetic reactors

are places in which the occasion occurs for genetic evol-

ution, particularly because of high biological connectivity,

generation of variation, and presence of specific selection.

Beyond mutational events, significant genetic variation

occurs as a consequence of recombinatorial events, fre-

quently resulting from genetic exchanges among organ-

isms inside populations and communities. There are four

main genetic reactors in which antibiotic resistance

evolves (Figure 1). The primary reactor is constituted

by the human and animal microbiota, with more than 500

bacterial species involved, in which therapeutic or pre-

ventive antibiotics exert their actions. The secondary

reactor involves the hospitals, long-term care facilities,

farms, or any other place in which susceptible individuals

are crowded and exposed to bacterial exchange. The

tertiary reactor corresponds to the wastewater and any

type of biological residues originated in the secondary

reactor, including for instance lagoons, sewage treatment

plants, or compost toilets, in which bacterial organisms

from many different individuals have the opportunity to

mix and genetically react. The fourth reactor is the soil

and the surface or ground water environments, where the

bacterial organisms originated in the previous reactors

mix and counteract with environmental organisms. Water

is involved as a crucial agent in all four genetic reactors,

but particularly in the last ones. The possibility of redu-

cing the evolvability of antibiotic resistance depends on

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http://dx.doi.org/10.1016/j.copbio.2008.05.006

Antibiotics and antibiotic resistance in water environments Baquero, Martınez and Canton 261

Figure 1

The four genetic reactors in antibiotic resistance, where genetic

exchange and recombination shapes the future evolution of resistance

determinants. Particularly in the lowest reactors, bacteria from human-

associated or animal-associated microbiota (in black) mix with

environmental bacteria (in white), increasing the power of genetic

variation and possible emergence of novel mechanisms of resistance

that are re-introduced in human or animal environments (back arrows).

the ability of humans to control the flow of active anti-

microbial agents, bacterial clones, and genetically based

biological information along these genetic reactors.

Industrial antibiotics in soil–waterenvironmentsWater dissolves industrial antibiotics that are bound to

environmental matrices. Binding to soil particles (and

sediments) delays its biodegradation and explains long-

term permanence of the drugs in the environment. Of

course, soil particles also remove antibiotics from water,

so that a kind of water–soil pharmacokinetics might be

considered. Antimicrobial agents are retained in soil by its

association with soil chemicals. For instance, Elliot soil

humic acids produce complexation of antibiotics [5].

Interestingly, heavy metals (as methyl-mercury) also

associate with humic acids, so that in the water film

associated with soil organic particles several antimicrobial

effects might be simultaneously present. Indeed it

appears that in the presence of humic substances, in both

dissolved and mineral-bound forms, environmental mobi-

lity of antibiotics [5] might increase. Aluminum and iron

oxides might alter these interactions by changing surface

charge. For instance, sorption to such oxides results in

different types of ciprofloxacin-surface complexes [5]


probably changing the reactivity of fluoroquinolones in

the soil–water interphase. It is to be noticed that general

alterations in water or in soil (as pH changes, or ionic

strength) might alter these antibiotic–soil–water inter-

actions, producing different levels of antibiotic release

(dissolution) from soil particles. In a study, half-lives in

soil have been estimated in 20–30 days for erythromycin

or oleandomycin.

Industrial antibiotics in water–sludgeenvironmentsAntimicrobial agents as sulfonamides, macrolides, tri-

methoprim, cephalosporins, or fluoroquinolones can be

found at potentially active concentrations in activated

sludge treatment, and the antibiotic load along the year

correlates with the variation in annual consumption data,

being higher in the winter [6]. The wastewater concen-

tration of antimicrobials depends on the sludge–waste-

water partition coefficient, but with fluoroquinolones field

experiments of sludge application to agricultural land

confirmed long persistence of these compounds, but with

limited mobility into the subsoil [7]. Very high concen-

trations of sulfonamides (20 � 103 ng/ml) have been

found in pig farm wastewater, and detection of sulfa-

methazine has been suggested to serve as a marker for

livestock-source contamination in Vietnam [8]. In Japa-

nese urban rivers a high number of antibiotic agents can

be detected, including sulfonamides, trimethoprim, and

macrolides. In Hong Kong and Shenzhen sewage

samples, penicillin levels (as penicillin V) were undetect-

able, but that was not the case for cephalosporins, as

cefalexin or cefotaxime reached concentrations exceed-

ing 1 mg/ml [9], probably sufficient to select organisms

producing extended-spectrum beta-lactamases, as CTX-

M enzymes. If selection of ESBL organism will produce a

reduction in the antibiotic concentration is controversial.

In compost toilets, amoxicillin decay is negligible, even in

the presence of beta-lactamase producing bacteria.

Hydrophobic antibiotics, as tetracycline or ciprofloxacin

were detected in all sludge samples from two Oslo city

hospitals, but not in the collected influent samples,

suggesting binding to effluent particles [10]. Similarly,

fluoroquinolones were consistently found in hospital

effluents [11�]. The extensive use of antibiotics in human

medicine, animal farming, and agriculture leads to anti-

biotic contamination of manure, which can be used as

fertilizer. Leaching tests indicate that in general less than

1% of fluoroquinolones in the sludge reached the aqueous

phase, which might indicate a relatively reduced mobility

when sludge is used to fertilize soil [7]. Nevertheless, that

does not exclude localized biological effects on particu-

lated material. Indeed high concentrations of fluoroqui-

nolones were found in secondary sludge (sorption).

Macrolides were frequently resistant to the processes

carried out in sewage treatment plants in South China,

and even higher concentrations were found in the final

effluents than in the raw sewages [12].


262 Environmental Biotechnology

Water disinfection and wastewater treatmentinfluence antibiotic concentrationsWater disinfection by ClO(2) might contribute to the

removal to beta-lactam agents. The water-degradation

of beta-lactams (penicillin G) has been recently explored,

being penicilloic acid the main degradation product [13].

Aqueous chlorination of drinking water and wastewater

removes trimethoprim activity [14]. Wastewater treat-

ment might eliminate nearly 80% of fluoroquinolones

or tetracyclines before they enter rivers, and are suscept-

ible to photodegradation [7,9]. Antibiotic removal effi-

ciencies by wastewater treatment are less effective for

macrolides that are relatively persistent in the environ-

ment [9]. The application of techniques for antibiotic

removal by coagulation and granular activated carbon

filtration, ionic treatment or micelle–clay systems are

promising for the removal of tetracycline and sulfona-

mides [15].

Measuring water-antibiotic concentrationsThe progress in instrumental analytical chemistry, using

electrophoretic and chromatographic techniques, as

liquid chromatography–tandem mass spectrometry

enables to detect many different types of antibiotics at

concentrations of nanograms/liter, after solid-phase

extraction [16,17]. Alternatively, immunochemical

approaches are also useful for inexpensive quick screen-

ing [17]. Voltammetry and amperometric detection of

tetracyclines using multiwall carbon nanotube modified

electrodes have been recently proposed for monitoring

water samples [18]. Even commercially available test kits

have been successfully used for rapid screening of anti-

biotic activity in effluents and surface water samples [19].

It is to be noticed that natural organic matter might

significantly impact the results of the analysis of some

antibiotics.

Reducing antibiotic-resistant bacteria inwastewaterAntibiotic-resistant organisms from humans and animals

are released into the sewage by contaminated sites (in-

cluding urine), feces, eventually corpses and manure. In

particular, wastewater from hospitals and intensive farm-

ing facilities (under concentrated animal feeding oper-

ations) is probably a major source of pathogenic and

antibiotic-resistant organisms and antibiotic-resistance

genes that are released into the environment. It is essen-

tial to increase our knowledge on effective barrier

measures preventing the incorporation of resistant and

pathogenic bacteria into the environment (see Introduc-

tion). Wastewater could be disinfected in many ways,

including chlorine (2–3 logs bacterial reduction with

chlorine dose of 30 mg/L), ozone (3–4 logs reduction at

100 mg/L), or ultraviolet light (effective but expensive)

[20]. These treatments might differ in different circum-

stances, as for instance ammonia present in wastewaters

might compete for free chlorine to form monochloramine.


In these cases effective chlorine doses might require

concentrations of 100 mg/L. Filtering technologies in-

cluding surface-modified ones activated carbon filter

media are promising (more than 6 logs reduction). The

results of some studies [20] indicate the possibility that

chlorination might result in the alteration of wastewater

populations, with the selection of chlorine-resistant bac-

teria (related to Bacillus subtilis and Bacillus licheniformis),which might contribute to the selection of particular

resistance genes and genetic platforms. A number of

studies have addressed the influence of different types

of manure management into the environmental fate of

resistance genes. High-intensity manure management

(with amending, watering, and turning) was more effec-

tive in reducing permanence of resistance genes than low-

intensity management. Different genes had diverse

kinetics of maintenance [21,22,23�], probably in relation

to the organisms harboring them.

Influence of water-antibiotics on antibioticresistanceLand application of manure can result in the dispersion of

resistant bacteria to water sources. The effect of a con-

centrated swine feeding operation on surface water and

groundwater situated up and down gradient of the swine

facility was studied [24]. The proportion of macrolide and

tetracycline-resistant enterococci was significantly

increased in down-gradient surface waters. Similarly,

samples of surface water sites near wastewater treatment

plants in Australia had a significant increase of antibiotic-

resistant Escherichia coli [25]. Nevertheless, the quanti-

tation of the effects of antibiotics on water bacteria

remains a difficult question, which has been addressed

by using model systems as mesocosms, soil-filled lysi-

meters representing the leachfield of a septic system.

Under these conditions, the local release of tetracycline

(5 mg/ml) had a very small effect in this model on the

development of antibiotic resistance [26�]. In another

model, using river water in continuous flow chemostat

system, similar results were found, but with high tetra-

cycline concentrations a greater diversity of tetracycline-

resistance genes was detected [27]. In a third model, using

a soil microcosm supplemented with pig manure slurry

and an Enterococcus faecalis strain harboring a tet(M) resist-

ance gene, stable tetracycline concentrations were unable

to influence the local prevalence of antibiotic-resistant

bacteria, but tetracycline-resistance genes persisted for a

long time, probably because of horizontal gene transfer to

other organisms. Obviously these models do not take into

account the possible concentration of drugs and bacteria

in particulated surfaces or sediments. A final concern

regards the utilization of prophylactic antibiotics in aqua-

culture. The heavy use of these compounds, several of

which are nonbiodegradable increases antibiotic selective

pressure in water, facilitates the transfer of antibiotic-

resistance determinants between aquatic bacteria,

including fish and human pathogens, and allows the



presence of residual antibiotics in commercialized fish

and shellfish products [2].

Antibiotic-resistant bacteria in waterWater bacteria might be indigenous to aquatic environ-

ments, or exogenous, transiently and occasionally present

in the water as a result of shedding from animal, vegetal,

or soil surfaces. More than 90% of bacterial strains origi-

nated in seawater are resistant to more than one antibiotic,

and 20% are resistant at least to five [28]. The study of

antibiotic resistance in indigenous water organisms is

important, as it might indicate the extent of alteration

of water ecosystems by human action. Aeromonas strains

from Portuguese estuarine water carry less frequently

beta-lactamase genes than Enterobacteriaceae (10% ver-

sus 78%) [29]. In water reservoirs a-half of Aeromonasstrains might present multiple antibiotic resistance [30].

Resistance profiles of aquatic pseudomonads depend on

the species composition, but also from the site in which

they were isolated, being more antibiotic-resistant along

shorelines and in sheltered bays than in the open water,

indicating the influence of nonaquatic organisms or pol-

lutants. Nevertheless, such influences can be found in the

more remote water environments; psychrotrophic bac-

teria from Antarctic show various degrees of resistance

to industrial antibiotics and metals [31]. The association

of antibiotic-resistance and resistance to heavy metals is

very frequent in the same organism (also in the same

plasmid, transposon, or integron) so that industrial pollu-

tion probably selects for antibiotic-resistance and viceversa [32�]. Indeed metal contamination represents a

long-standing, widespread, and recalcitrant selection

pressure for multiresistant organisms. For the nonaquatic

organisms, obviously the density of antibiotic-resistance

organisms and antibiotic-resistance genes in fresh water

varies with the proximity to areas with increased anti-

biotic consumption, metal pollution, and between sea-

sons, being more frequently found in rainy seasons [23�].Very little work has been done to elucidate the role of

bacterial biofilms in water environments and its role in

antibiotic resistance. Phenotypic antibiotic resistance in

bacterial biofilms might indeed protect the water environ-

ment from selective events caused by the antibiotic

release, which probably are acting more effectively on

planktonic bacteria.

Tracking the sources for antibiotic-resistantorganisms in waterThe accessibility of modern molecular techniques for

subspecific characterization of bacterial organisms (clonal

detection) should readily increase our possibilities for

antibiotic-resistance microbial source tracking. Such

approach will provide only useful results after a much

more comprehensive knowledge of population biology of

bacterial organisms, as the genetic diversity of potential

organisms entering in water is very high [33]. The same is

true for tracking the plasmids and other genetic mobile


platforms involved in antibiotic resistance, but it is clear

that genetic techniques are providing a much more accu-

rate image of the real diversity and complexity of anti-

biotic resistance in water-borne bacteria, if compared with

cultivation-depending approaches [29]. Nevertheless, for

local purposes, phenotypic techniques, as those based on

carbon-utilization and antibiotic-resistance patterns

might still be useful for bacterial source tracking [34].

Horizontal gene transfer of antibioticresistance in water environmentsEstuarine water-borne Aeromonas strains carry almost as

frequently as Enterobacteriaceae class 1 integron plat-

forms carrying antibiotic-resistance genes [29]. Exclu-

sively environmentally based organisms, as Delftia, also

harbor class 3 integrons [35�]. The persistence of such

genetic structures cannot probably be explained solely by

antibiotic selection, suggesting that activities resulting in

antibiotic resistance might have other physiological roles,

or that they are placed in multifunctional plasmids. The

most frequent gene cassette found involves aminoglyco-

side-resistance genes, rarely under positive selection in

our days, and there is a suspicion that some other resist-

ance genes, as integron sul genes, might provide benefits

for the bacteria, unrelated with resistance. However,

some of these mobile gene cassettes in Aeromonas might

involve important mechanisms of resistance, as Qnr,

involved in fluoroquinolone resistance, which might be

horizontally propagated by IncU-type plasmids [36�].Certainly the dense bacterial populations in sewage treat-

ment plants favor genetic exchange among bacterial

populations and communities, integrons predating trans-

posons and plasmid dissemination. Multiresistance plas-

mids of broad host-range are consistently recovered in

sewage [37]. Interestingly, antibiotic-resistance genes

from manure influence the lagoons and groundwater gene

pool, but this pool also contains antibiotic-resistance

genes from indigenous bacteria [38]. Aeromonas from

aquaculture water systems (fish, eel farming) are particu-

larly resistant to antibiotics [39], and frequently contain

plasmids and integrons with multiple genes for antibiotic

resistance [40], and the association with heavy-metal

resistance is not uncommon [32�]. Water originated in

transgenic plant fields may constitute a matter of concern,

but no significant differences have been found in bacterial

antibiotic-resistance levels between transgenic and non-

transgenic corn fields [41].

Environmental damage mediated byantibiotics in water environmentsPharmaceuticals are introduced in the environment from

human and veterinary applications at volumes comparable

with total pesticide loadings [42�]. Antibiotic resistance is

not the only possible adverse effect of antibiotic release in

water environments, and ecotoxicity tests are starting to be

introduced to document these effects [43]. Antibiotics

might act, at very low concentrations, as signaling agents


264 Environmental Biotechnology

(a kind of hormones) in microbial environments [44–46].

Common receptors have been identified in plants for a

number of antibiotics and disinfectants affecting chloro-

plast replication (fluoroquinolones), transcription–trans-

lation (tetracyclines, macrolides, lincosamides,

aminoglycosides, pleuromutilins), folate biosynthesis (sul-

fonamides, and probably trimetoprim), fatty acid synthesis

(triclosan), and sterol biosynthesis (azoles, statins) [42�].During the past years the environmental consequences of

the release of triclosan in freshwater environment has been

considered [47]. Ciprofloxacin affects stream microbial

communities, including those colonizing senesced leaf

materials [48]. A matter of major future concern is the

effect of antibiotics and disinfectants released into the

environment on Cyanobacteria, largely susceptible to anti-

microbial agents, as such type of organisms accounts for

more than 70% of the total phytoplankton mass, and are

responsible for more than a third of the total free O2

production, or CO2 fixation. Amazonia is green, visible,

and attractive, but there are much bigger microscopic

Amazonias! What seems certain is that such alterations

in microbial ecosystems, either produced by antimicrobial

release or by the unexpected effective dispersal in water

environments of resistant pathogenic organisms [49] might

be relevant for public health. Future prediction and pre-

vention of antibiotic resistance [50] depends on the

research investments in the ecology, including water

ecology, of antibiotic-resistant microorganisms.

ConclusionsAn important part of the dispersal and evolution of anti-

biotic-resistant bacterial organisms depends on water

environments. In water, bacteria from different origins

(human, animal, environmental) are able to mix, and

resistance evolves as a consequence of promiscuous

exchange and shuffling of genes, genetic platforms, and

genetic vectors. At the same time, antibiotics, disinfec-

tants, and heavy metals are released in water, and might

exert selective activities, as well as ecological damage in

water communities, resulting in antibiotic resistance.

Methods should be developed for cheap and reliable: first,

bacterial clones and resistance genes source tracking; sec-

ond, detection of antibiotics in water environments; third,

disinfection of water from antibiotic-resistant populations

and the resistance gene pool, and removal of antibiotics

from wastewater; and fourth, prevention policies for mixing

human–animal-originated and soil–water bacteria.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

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2. Cabello FC: Heavy use of prophylactic antibiotics inaquaculture: a growing problem for human and animal healthand for the environment. Environ Microbiol 2006, 8:1137-1144.


3. D’Acosta VM, McGrann KM, Hughes DW, Wright GD: Samplingthe antibiotic resistome. Science 2006, 311:374-377.

4. Kim S, Aga DS: Potential ecological and human health impactsof antibiotics and antibiotic-resistant bacteria fromwastewater treatment plants. J Toxicol Environ Health B: CritRev 2007, 10:559-573.

5. Gu C, Karthikeyan KG: Sorption of the antibiotic tetracyclineto humic–mineral complexes. J Environ Qual 2008,37:704-711.

6. Gobel A, Thomsen A, McArdell CS, Joss A, Giger W: Occurrenceand sorption behavior of sulfonamides, macrolides, andtrimethoprim in activated sludge treatment. Environ SciTechnol 2005, 39:3981-3989.

7. Sukul P, Spiteller M: Fluoroquinolone antibiotics in theenvironment. Rev Environ Contam Toxicol 2007,191:131-162.

8. Managaki S, Murata A, Takada H, Tuyen BC, Chiem NH:Distribution of macrolides, sulfonamides and trimethoprim intropical waters: ubiquitous occurrence of veterinaryantibiotics in the Mekong delta. Environ Sci Technol 2007,41:8004-8010.

9. Gulkowska A, Leung HW, So MK, Taniyasu S, Yamashita N,Yeung LW, Richardson BJ, Lei AP, Giesy JP, Lam PK: Removal ofantibiotics from wastewater by sewage treatment facilities inHong Kong and Shenzhen, China. Water Res 2008, 42:395-403.

10. Thomas KV, Dye C, Schlabach M, Langford KH: Source to sinktracking of selected human pharmaceuticals from two Oslocity hospitals and a wastewater treatment works. J EnvironMonit 2007, 12:1410-1418.

11.�

Lindberg RH, Bjorklund K, Rendahl P, Johansson MI, Tysklind M,Andersson BA: Environmental risk assessment with emphasison sewage treatment plants. Water Res 2007, 41:613-619.

A synthetic view of the environmental effects of antibiotics and itspotential risks.

12. Xu W, Zhang G, Li X, Zou S, Li P, Hu Z, Li J: Occurrence andelimination of antibiotics at four sewage treatment plants inthe Pearl River Delta, South China. Water Res 2007, 19:4526-4534.

13. Li D, Yang M, Hu J, Zhang Y, Chang H, Jin F: Determination ofpenicillin G and its degradation products in a penicillinproduction wastewater treatment plant and the receivingriver. Water Res 2008, 42:307-317.

14. Dodd MC, Huang CH: Aqueous chlorination of the antibioticagent trimethoprim: reaction kinetics and pathways. WaterRes 2007, 41:647-655.

15. Choi KJ, Kim SG, Kim SH: Removal of antibiotics by coagulationand granular activated carbon filtration. J Hazard Mater 2008,151:38-43.

16. Dıaz-Cruz MS, Barcelo D: Determination of antimicrobialresidues and metabolites in the aquatic environment by liquidchromatography tandem mass spectrometry. Anal BioanalChem 2006, 386:973-985.

17. Buchberger WW: Novel analytical procedures for screening ofdrug residues in water, wastewater, sediment, and sludge.Anal Chim Acta 2007, 19:129-139.

18. Vega D, Agui L, Gonzalez-Cortes A, Yanez-Sedeno P,Pingarron JM: Voltammetry and amperometric detection oftetracyclines at multi-wall carbon nanotube modifiedelectrodes. Anal Bioanal Chem 2007, 389:951-958.

19. Smith AJ, Balaam JL, Ward A: The development of a rapidscreening technique to measure antibiotic activity ineffluents and surface water samples. Mar Pollut Bull 2007,54:1940-1946.

20. Macauley JJ, Quiang Z, Adams CD, Surampalli R, Mormile MR:Disinfection of swine wastewater using chlorine, ultravioletlight and ozone. Water Res 2006, 10:2017-2026.

21. Pei R, Cha J, Carlson KH, Pruden A: Response of antibioticresistance genes to biological treatment in dairy lagoon water.Environ Sci Technol 2007, 41:5108-5113.



22. Auerbach EA, Seyfried EE, McMahon KD: Tetracyclineresistance genes in activated sludge wastewater treatmentplants. Water Res 2007, 41:1143-1151.

23.�

Peak N, Knapp CW, Yang RK, Hanfelt MM, Smith MS, Aga DS,Graham DW: Abundance of six tetracycline resistancegenes in wastewater lagoons at cattle feedlots withdifferent antibiotic use strategies. Environ Microbiol 2007,9:143-151.

The approach of this paper is to explore gene diversity instead oforganism diversity in contaminated water, and how this ‘gene populationbiology’ is altered by the use of antibiotics.

24. Sapkota AR, Curriero FC, Gibson KE, Schwab KJ: Antibiotic-resistant enterococci and fecal indicators in surface water andgroundwater impacted by a concentrated Swine feedingoperation. Environ Health Perspect 2007, 115:1040-1045.

25. Watkinson AJ, Micalizzi GR, Bates JR, Costanzo SD: Novelmethod for rapid assessment of antibiotic resistance inEscherichia coli isolates from environmental waters by use ofa modified chromogenic agar. Appl Environ Microbiol 2007,73:2224-2229.

26.�

Atoyan JA, Patenaude EL, Potts DA, Amador JA: Effects oftetracycline on antibiotic resistance and removal of fecalindicator bacteria in aerated and unaerated leachfieldmesocosms. J Environ Sci Health A: Tox Hazard Subst EnvironEng 2007, 42:1571-1578.

This paper proposes the use of model systems to predict the environ-mental effect of antibiotic release in wastewater treatment facilities.

27. Munoz-Aguayo J, Lang KS, LaPara TM, Gonzalez G, Singer RS:Evaluating the effects of chlortetracycline on the proliferationof antibiotic-resistant bacteria in a simulated river waterecosystem. Appl Environ Microbiol 2007, 17:5421-5425.

28. Martinez JL: Recent advances on antibiotic resistance genes.In Recent Advances in Marine Biotechnology. Molecular Geneticsof Marine Organisms, vol 10. Edited by Fingerman,Nagabhushanam. 2003:13-32.

29. Henriques IS, Fonseca F, Alves A, Saavedra MJ, Correia A:Occurrence and diversity of integrons and beta-lactamasegenes among ampicillin-resistant isolates from estuarinewaters. Res Microbiol 2006, 157:938-947.

30. Blasco MD, Esteve C, Alcaide E: Multiresistant waterbornepathogens isolated from water reservoirs and coolingsystems. J Appl Microbiol 2008.

31. De Souza MJ, Nair S, Loka Bharati PA, Chandramohan D: Metaland antibiotic resistance in psychotrophic bacteria fromAntarctic marine waters. Ecotoxicology 2006, 15:379-384.

32.�

Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV: Co-selection of antibiotic and metal resistance. Trends Microbiol2006, 14:176-182.

This is an excellent review of the role of metal pollution in selectingantibiotic resistance and vice versa.

33. Olivas Y, Faulkner BR: Fecal source tracking by antibioticresistance analysis on a watershed exhibiting low resistance.Environ Monit Assess 2008, 139:15-25.

34. Moussa SH, Massengale RD: Identification of the sources ofEscherichia coli in a watershed using carbon-utilizationpatterns and composite data sets. J Water Health 2008,6:197-207.

35.�

Xu H, Davies J, Miao V: Molecular characterization of class 3integrons from Delftia spp. J Bacteriol 2007, 189:6276-6283.

The investigation of the integron dispersal in environmental bacterialcommunities is crucial to understand the antibiotic-resistance geneflow among free-leaving and human-associated or animal-associatedbacteria.

36.�

Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P:Unexpected occurrence of plasmid-mediated quinolone


resistance determinants in environmental Aeromonas spp.Emerg Infect Dis 2008, 14:231-237.

This group of authors explore in this and other papers the origin ofclinically relevant antibiotic resistances in environmental bacteria.

37. Schluter A, Szczepanowski R, Kurz N, Schneiker S, Krahn I,Puhler A: Erythromycin resistance-conferring plasmidpRSB105, isolated from a sewage treatment plant, harbors anew macrolide resistance determinant, an integron-containing Tn402-like element, and a large region of unknownfunction. Appl Environ Microbiol 2007, 73:1952-1960.

38. Koike S, Krapac IG, Oliver HD, Yannarell AC, Chee-Sanford JC,Aminov RI, Mackie RI: Monitoring and source tracking oftetracycline resistance genes in lagoons and groundwateradjacent to swine production facilities over a 3-year period.Appl Environ Microbiol 2007, 73:4813-4823.

39. Penders J, Stobbering EE: Antibiotic resistance of motileaeromonads in indoor catfish and eel farms in the southernpart of The Netherlands. Int J Antimicrob Agents 2007,31:261-265.

40. Jacobs L, Chenia HY: Characterization of integrons andtetracycline resistance determinants in Aeromonas spp.isolated from South African aquaculture systems. Int J FoodMicrobiol 2007, 114:295-306.

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42.�

Brain RA, Hanson ML, Solomon KR, Brooks BW: Aquatic plantsexposed to pharmaceuticals: effects and risks. Rev EnvironContam Toxicol 2008, 192:67-115.

This paper deals with larger ecological and environmental effects ofpharmaceuticals, and particularly antibiotics.

43. Yamashita N, Yasojima M, Nakada N, Miyajima K, Komori K,Suzuki Y, Tanaka H: Effects of antibacterial agents,levofloxacin and clarithromycin, on aquatic organisms. WaterSci Technol 2006, 53:65-72.

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45. Linares JF, Gustafsson I, Baquero F, Martinez JL: Antibiotics asintermicrobial signaling agents instead of weapons. Proc NatlAcad Sci U S A 2006, 103:19484-19489.

46. Fajardo A, Martınez-Martın N, Mercadillo M, Galan JC, Ghysels B,Matthijs S, Cornelis P, Wiehlmann L, Tummler, Baquero F,Martınez JL: The neglected intrinsic resistome of bacterialpathogens. PLoS ONE 2008, 3:e1619.

This paper reveals the wealth of genes potentially involved not only inantibiotic resistance in bacterial pathogens but also in environmentalorganisms, genes able to contribute to the evolution of antibioticresistance.

47. Capdevielle M, van Egmond R, Whelan M, Versteeg D, Hofmann-Kamensky M, Inauen J, Cunningham V, Woltering D:Consideration of exposure and species sensitivity of triclosanin the freshwater environment. Integr Environ Assess 2008,4:15-23.

48. Maul JD, Schuler LJ, Beiden JB, Whiles MR, Lydy MJ: Effects ofthe antibiotic ciprofloxacin on stream microbial communitiesand detritivorous macroinvertebrates. Environ Toxicol Chem2006, 25:1598-1606.

49. Quinteira S, Peixe L: Multiniche screening reveals the clinicallyrelevant metallo-beta-lactamase VIM-2 in Pseudomonasaeruginosa far from the hospital setting: an ongoingdispersion process? Appl Environ Microbiol 2006, 72:3743-3745.

50. Martınez JL, Baquero F, Andersson DI: Predicting antibioticresistance. Nat Rev Microbiol 2007, 5:958-965.


antibiotics and antibiotic resistance in water environments

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