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Antibiotics and Antibiotic Resistance in Water Environments

  • Ramón y Cajal University Hospital - Ramón y Cajal Institute for Health Research, IRYCIS.

Abstract and Figures

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.
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Antibiotics and antibiotic resistance in water environments
Fernando Baquero
, Jose
´-Luis Martı
and Rafael Canto
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.
Department of Microbiology, Ramo
´n y Cajal University Hospital,
National Center for Biotechnology, CSIC, Spain
Joint Unit for Antimicrobial Resistance and Virulence, 28034 Madrid,
Corresponding author: Baquero, Fernando (
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
Human 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 antibiotic
Antibiotic 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
Current Opinion in Biotechnology 2008, 19:260–265
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–water
Water 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–sludge
Antimicrobial 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 10
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].
Antibiotics and antibiotic resistance in water environments Baquero, Martı
´nez and Canto
´n 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). Current Opinion in Biotechnology 2008, 19:260–265
Water disinfection and wastewater treatment
influence antibiotic concentrations
Water 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 concentrations
The 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
Reducing antibiotic-resistant bacteria in
Antibiotic-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 antibiotic
Land 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
262 Environmental Biotechnology
Current Opinion in Biotechnology 2008, 19:260–265
presence of residual antibiotics in commercialized fish
and shellfish products [2].
Antibiotic-resistant bacteria in water
Water 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 Aeromonas
strains 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 vice
versa [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-resistant
organisms in water
The 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 antibiotic
resistance in water environments
Estuarine 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 by
antibiotics in water environments
Pharmaceuticals 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
Antibiotics and antibiotic resistance in water environments Baquero, Martı
´nez and Canto
´n 263 Current Opinion in Biotechnology 2008, 19:260–265
(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 O
production, or CO
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.
An 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 reading
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have been highlighted as:
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communities is crucial to understand the antibiotic-resistance gene
flow among free-leaving and human-associated or animal-associated
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 of
clinically relevant antibiotic resistances in environmental bacteria.
37. Schlu
¨ter A, Szczepanowski R, Kurz N, Schneiker S, Krahn I,
¨hler A: Erythromycin resistance-conferring plasmid
pRSB105, isolated from a sewage treatment plant, harbors a
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containing Tn402-like element, and a large region of unknown
function.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 of
tetracycline resistance genes in lagoons and groundwater
adjacent to swine production facilities over a 3-year period.
Appl Environ Microbiol 2007, 73:4813-4823.
39. Penders J, Stobbering EE: Antibiotic resistance of motile
aeromonads in indoor catfish and eel farms in the southern
part of The Netherlands.Int J Antimicrob Agents 2007,
40. Jacobs L, Chenia HY: Characterization of integrons and
tetracycline resistance determinants in Aeromonas spp.
isolated from South African aquaculture systems.Int J Food
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41. Demane
´che S, Sanguin H, Pote
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soil bacteria in transgenic plant fields.Proc Natl Acad Sci U S A
2008, 105:3957-3962.
Brain RA, Hanson ML, Solomon KR, Brooks BW: Aquatic plants
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Contam Toxicol 2008, 192:67-115.
This paper deals with larger ecological and environmental effects of
pharmaceuticals, 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.Water
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44. Fajardo A, Martı
´nez JL: Antibiotics as signals that trigger
specific bacterial responses.Curr Opin Microbiol 2008,
45. Linares JF, Gustafsson I, Baquero F, Martinez JL: Antibiotics as
intermicrobial signaling agents instead of weapons.Proc Natl
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46. Fajardo A, Martı
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Matthijs S, Cornelis P, Wiehlmann L, Tu
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´nez JL: The neglected intrinsic resistome of bacterial
pathogens.PLoS ONE 2008, 3:e1619.
This paper reveals the wealth of genes potentially involved not only in
antibiotic resistance in bacterial pathogens but also in environmental
organisms, genes able to contribute to the evolution of antibiotic
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 triclosan
in the freshwater environment.Integr Environ Assess 2008,
48. Maul JD, Schuler LJ, Beiden JB, Whiles MR, Lydy MJ: Effects of
the antibiotic ciprofloxacin on stream microbial communities
and detritivorous macroinvertebrates.Environ Toxicol Chem
2006, 25:1598-1606.
49. Quinteira S, Peixe L: Multiniche screening reveals the clinically
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Antibiotics and antibiotic resistance in water environments Baquero, Martı
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... Multiple studies have demonstrated that irrational antibiotics are being prescribed by physicians, general people have a habit of self-medication, and there is also an indiscriminate use of antibiotics in agriculture and farming in different parts of the country (Biswas et al., 2014;Mostafa Shamsuzzaman & Kumar Biswas, 2012 animal and industrial effluents and create a reservoir of bacteria (Adelowo et al., 2018;Sibanda et al., 2015). This contaminated ecosystem provides optimum conditions to antibiotic resistant bacteria from various sources to mix and transfer their resistant gene(s) to clinically important bacteria for development of human pathogens with novel resistance mechanisms (Baquero et al., 2008;Maravić et al., 2016;Tacão et al., 2012). ...
... -35 -Although, it is important to monitor the occurrence of ARGs in highly polluted environments where high selection pressure exerted by antimicrobial contaminants contribute toward the spread and persistence of antibioticresistant bacteria, it is critical not to ignore the emergence of ARGs in relatively less polluted environments (Baquero et al., 2008;Martinez, 2009;Williams, 2001). Identifying sources of ARGs and their dissemination in relatively less polluted environments will help form strategies to reduce their spread. ...
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The aquatic environment of river water is the most intensively human influenced ecosystem in the world as it receives huge amount of urban, hospital, animal and industrial effluents and create a reservoir of diverse type of bacteria. This contaminated ecosystem provides optimum conditions to antibiotic resistant bacteria from various sources to mix and transfer their resistant gene(s) to clinically important bacteria for development of human pathogens with novel resistance mechanisms. Hospital wastewater, in particular, is expected to contain high abundances of antibiotic resistance genes (ARGs) as it contains human enteric bacteria that may include antibiotic-resistant organisms originating from hospital patients, and can also have high concentrations of antibiotics and antimicrobials that facilitate the environmental spread of antibiotic resistance. Therefore, in this study, we applied 16S rRNA gene sequencing, a culture-independent method to analyze bacterial diversity present in river as well as hospital wastewater. River and hospital wastewater were collected from Dhaka, Bangladesh and sequenced for V3 and V4 region of 16S rRNA gene resulting in a total of 36 sequence libraries. In total 4,13,297 sequence reads were obtained where the number of sequence reads ranged from 1333 to 38110 reads per library. The taxonomic analysis revealed 8 phyla, 12 classes, 13 orders, 22 families and 102 genera present in the river and hospital wastewater samples. Additionally, permutational multivariate analysis of variance (PERMANOVA) of bacterial membership in terms of Bray-Curtis, based on operational taxonomic unit (OTUs) at a 97% sequence similarity threshold showed significant bacterial diversity between river and hospital wastewater. Moreover, compositions and relative abundance of the bacterial genera showed the presence of most pathogenic bacteria, mostly in the hospital wastewater. We performed another study to analyze blaCTX-M variants for their extensively emerging clinical importance. The presence of blaCTX-Mgene in the bacteria producing extended spectrum beta lactamases (ESBLs) has made it resistant to the broad-spectrum third-generation cephalosporin antibiotics that are used in hospitals to treat infections of the skin and respiratory tract caused by both Gram negative and Gram positive bacteria. The river and hospital wastewater were sequenced for ARG, resulting in a total of 33 sequence libraries. Out of 172 variants of blaCTX-M reported so far, our study found 124 variants, around 62% of which are present in hospital wastewater. The non-metric multidimensional scaling (NMDS) showed that there is close association among the blaCTX-M variants present in hospital wastewater whereas the variants for river water is scattered through the sampling sites. Overall, the findings of our study indicated that river and hospital wastewater contains diverse types of bacteria where the bacterial community from river water significantly differs from that of hospital wastewater. Both of the sampling site contains multidrug resistant bacterial genera that may pose serious threat to the aquatic environment of river water resulting in a serious public health burden. Moreover, the presence of significant number of blaCTX-M variants may facilitate the global burden of antimicrobial resistance.
... An examination of the presence of antibiotic resistance in native aquatic species is significant as it can reveal how human activity alters aquatic ecosystems (Baquero et al. 2008). Antimicrobial antibiotic accumulations in edible tissues can result in allergies and harmful effects, changes to the gut microbial fauna, and development of medication resistance . ...
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The fisheries sub-sector of aquaculture—i.e., the pisciculture industry, contributes significantly to a country’s economy, employing a sizable proportion of the population. It also makes important contributions to household food security because the current demand for animal protein cannot be fulfilled by harvesting wild fish from riverines, lakes, dams, and oceans. For good pond management techniques and sustaining fish health, the fisherfolk, and the industry require well-established regulatory structures, efficient disease management strategies, and other extended services. In rearing marine fish, infections resulting from disease outbreaks are a weighty concern because they can cause considerable economic loss due to morbidity and mortality. Consequently, to find effective solutions for the prevention and control of the major diseases limiting fish production in aquaculture, multidisciplinary studies on the traits of potential fish pathogens, the biology of the fish as hosts, and an adequate understanding of the global environmental factors are fundamental. This review highlights the various bacterial diseases and their causative pathogens prevalent in the pisciculture industry and the current solutions while emphasising marine fish species. Given that preexisting methods are known to have several disadvantages, other sustainable alternatives like antimicrobial peptides, synthetic peptides, probiotics, and medicinal treatments have emerged to be an enormous potential solution to these challenges. Graphical abstract
... The propagation of ARGs into surrounding environments transforms antibiotic resistance becomes an environmental pollution issue, positioning ARG as a contaminant of emerging concern [77]. The accumulation of antimicrobial agents, detergents, disinfectants, heavy metals, and, other contaminants [78,79] could expedite the occurrence of ARBs and ARGs in different water bodies such as hospital waste effluents, water treatment plants, and tap water [80]. The ESKAPE group may be a relevant component of drug resistance distribution. ...
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ESKAPE bacteria represent a group of opportunistic bacterial pathogens that display widespread antimicrobial resistance, including resistance to the last-line antibiotics, thereby posing a significant clinical implication globally. Anthropogenic activities, such as wastewater from hospitals, livestock farms, crop fields, and wastewater treatment plants, contribute to the dissemination of antimicrobial-resistant bacterial pathogens into the environment. Surface water sources, including river waters, act as critical points of discharge for wastewater, pollutants, antibiotic-resistant bacteria (ARB), and antibiotic-resistant genes (ARG). These environmental factors, along with others, facilitate the dissemination and survival of ARBs, as well as promote the exchange of ARGs. Therefore, it is crucial to comprehend the current environmental landscape concerning the prevalence and persistence of resistant bacteria, particularly those belonging to the ESKAPE group. This review aims to provide a comprehensive overview of the current dissemination and characterization of ESKAPE bacteria in surface water and wastewater sources.
... ARGs are considered emerging contaminants in aquatic ecosystems (4), and the occurrence of ARGs in drinking water is a potential risk to human health (5). Groundwater and surface waters such as lakes and rivers are often used as source waters to drinking water treatment plants and are considered important reservoirs for antibiotic resistant bacteria (ARB) and associated ARGs (6)(7)(8). Drinking water treatment processes do not completely remove ARB and ARGs, which are subsequently transported through drinking water distribution systems (DWDS) (9,10). Drinking water disinfection processes use chlorine or chlora mines to inhibit microbial growth in distribution systems; however, exposure to chlorine and metals at subinhibitory concentrations can also select for antibiotic resistance in aquatic environments such as DWDS (11)(12)(13). ...
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Corrosion inhibitors, including zinc orthophosphate, sodium orthophosphate, and sodium silicate, are commonly used to prevent the corrosion of drinking water infrastructure. Metals such as zinc are known stressors for antibiotic resistance selection, and phosphates can increase microbial growth in drinking water distribution systems (DWDS). Yet, the influence of corrosion inhibitor type on antimicrobial resistance in DWDS is unknown. Here, we show that sodium silicates can decrease antibiotic resistant bacteria (ARB) and antibiotic-resistance genes (ARGs), while zinc orthophosphate increases ARB and ARGs in source water microbial communities. Based on controlled bench-scale studies, zinc orthophosphate addition significantly increased the abundance of ARB resistant to ciprofloxacin, sulfonamides, trimethoprim, and vancomycin, as well as the genes sul1 , qac EΔ1, an indication of resistance to quaternary ammonium compounds, and the integron-integrase gene intI 1. In contrast, sodium silicate dosage at 10 mg/L resulted in decreased bacterial growth and antibiotic resistance selection compared to the other corrosion inhibitor additions. Source water collected from the drinking water treatment plant intake pipe resulted in less significant changes in ARB and ARG abundance due to corrosion inhibitor addition compared to source water collected from the pier at the recreational beach. In tandem with the antibiotic resistance shifts, significant microbial community composition changes also occurred. Overall, the corrosion inhibitor sodium silicate resulted in the least selection for antibiotic resistance, which suggests it is the preferred corrosion inhibitor option for minimizing antibiotic resistance proliferation in DWDS. However, the selection of an appropriate corrosion inhibitor must also be appropriate for the water chemistry of the system (e.g., pH, alkalinity) to minimize metal leaching first and foremost and to adhere to the lead and copper rule. IMPORTANCE Antibiotic resistance is a growing public health concern across the globe and was recently labeled the silent pandemic. Scientists aim to identify the source of antibiotic resistance and control points to mitigate the spread of antibiotic resistance. Drinking water is a direct exposure route to humans and contains antibiotic-resistant bacteria and associated resistance genes. Corrosion inhibitors are added to prevent metallic pipes in distribution systems from corroding, and the type of corrosion inhibitor selected could also have implications on antibiotic resistance. Indeed, we found that sodium silicate can minimize selection of antibiotic resistance while phosphate-based corrosion inhibitors can promote antibiotic resistance. These findings indicate that sodium silicate is a preferred corrosion inhibitor choice for mitigation of antibiotic resistance.
Agricultural microbiomes are major reservoirs of antibiotic resistance genes (ARGs), posing continuous risks to human health. To understand the role of bacteriophages as vehicles for the horizontal transfer of ARGs in the agricultural microbiome, we investigated the diversity of bacterial and viral microbiota from fecal and environmental samples on an organic farm. The profiles of the microbiome indicated the highest abundance of Bacteroidetes, Firmicutes, and Proteobacteria phyla in animal feces, with varying Actinobacteria and Spirochaetes abundance across farm animals. The most predominant composition in environmental samples was the phylum Proteobacteria. Compared to the microbiome profiles, the trends in virome indicated much broader diversity with more specific signatures between the fecal and environmental samples. Overall, viruses belonging to the order Caudovirales were the most prevalent across the agricultural samples. Additionally, the similarities within and between fecal and environmental components of the agricultural environment based on ARG-associated bacteria alone were much lower than those of total microbiome composition. However, there were significant similarities in the profiles of ARG-associated viruses across the fecal and environmental components. Moreover, the predictive models of phage-bacterial interactions on bipartite ARG transfer networks indicated that phages belonging to the order Caudovirales, particularly in the Siphoviridae family, contained diverse ARG types in different samples. Their interaction with various bacterial hosts further implied the important role of bacteriophages in ARG transmission across bacterial populations. Our findings provided a novel insight into the potential mechanisms of phage-mediated ARG transmission and their correlation with resistome evolution in natural agricultural environments. IMPORTANCE Antibiotic resistance has become a serious health concern worldwide. The potential impact of viruses, bacteriophages in particular, on spreading antibiotic resistance genes is still controversial due to the complexity of bacteriophage-bacterial interactions within diverse environments. In this study, we determined the microbiome profiles and the potential antibiotic resistance gene (ARG) transfer between bacterial and viral populations in different agricultural samples using a high-resolution analysis of the metagenomes. The results of this study provide compelling genetic evidence for ARG transfer through bacteriophage-bacteria interactions, revealing the inherent risks associated with bacteriophage-mediated ARG transfer across the agricultural microbiome.
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By rationally adjusting the coordination environment and constructing the more electron‐enriched active site in single‐atom catalysts, the effect of heterogenous peroxymonosulfate (PMS)‐based Fenton‐like reactions can be effectively improved, yet remains a severe challenge. In this study, the electron‐rich Ru dual‐atom site is successfully immobilized onto N‐doped carbon (Ru2N6‐C) for PMS activation in water purification. The presence of electron‐rich Ru dual‐atom sites not only provides more electrons for PMS but also facilitates the formation of a Yeager adsorption configuration on the catalyst surface, which enhances O─O bond cleavage and leads to an increase in •SO4⁻ and •OH generation. Moreover, the Ru2N6‐C catalyst exhibits exceptional durability and reliability, achieving an ultra‐high efficiency with a turnover frequency of 153.95 min⁻¹ M⁻¹ for the naproxen degradation. A membrane reactor is further developed for the purification of wastewater, which is expected to provide a viable approach to controlling water pollution through the design of metal dual‐atom sites carbon‐based catalysts.
Melanophryniscus admirabilis is a microendemic and critically endangered toad, known from a single population. This microendemic species inhabits a small fragment of the Atlantic Forest in South Brazil, an area significantly impacted by hydroelectric power plant projects, livestock farming, agricultural activities, biopiracy, and tourism. Given the exclusive and limited population of M. admirabilis, preserving and conserving this species is of utmost importance in Brazil. Research on this species primarily concentrates on its biology, ecology, and ecotoxicology. Currently, there is no knowledge about antimicrobial resistance (AMR) bacteria present in wild M. admirabilis, despite the potential for studying them to provide valuable insights into environmental pollution. To this end, Enterobacteriaceae species (n = 82) obtained from 15 wild M. admirabilis toads were subjected to the standard Kirby–Bauer disk diffusion method to test their AMR. The results showed that Enterobacteriaceae species had the highest antibiotic resistance to IPM (45.1%), CIP (39%), NIT (32.5%), AMP (31.3%), TET (18.3%), and FOX (17%). Of the tested species, 18 (21.9%) species tested were susceptible, 40 (48.8%) were resistant to 1 or 2 different antibiotic classes, and 24 (29.3%) were classified as multidrug-resistant. Overall, our findings suggest that the incidence of AMR in Enterobacteriaceae isolated from wild M. admirabilis is high, indicating environmental stress caused by anthropic pollution in their habit.
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Antibiotic overuse in animal and human healthcare has led in the accumulation of potentially hazardous antibiotic residues, known as emerging contaminants. These residues contaminate animal products including meat, milk, and eggs, which humans then ingest. Furthermore, antibiotic residues from pharmaceutical firms, hospitals, and households reach wastewater treatment plants, providing an environment conducive to bacterial growth and dissemination. This, in turn, can result in the spread of antibiotic resistance genes (ARGs) among bacterial cells, posing serious threats to both human health and the environment. In the case of ARGs, conventional approaches for eliminating antibiotic residues from wastewater and aquatic habitats have proven ineffective. Recent study, however, has shown that the adsorption technique, particularly when low-cost and environmentally acceptable bioadsorbents such as sawdust, prawn shell waste, algae, and fungi are used, is highly successful in removing antibiotic residues. Bioadsorbents Microalgae, Terminalia catappa leaf, and siris seed pods, in particular, have shown outstanding removal efficiency for antibiotics such as tetracycline, dicloxacillin, and nitromidazole, reaching up to 98.74%. These investigations have shed insight on the fundamental principles of the adsorption process, revealing its ability to target ARGs and antibiotic-resistant bacteria as well as remove antibiotic residues. As a result, addressing the issue of antibiotic residues in the environment has become critical in order to protect human health and prevent the spread of antibiotic resistance. Adsorption, particularly when bioadsorbents are used, appears to be a promising and efficient method of combating antibiotic residues and limiting the spread of antibiotic resistance genes and antibiotic-resistant bacteria in aquatic settings.
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Microbial resistance to antibiotics currently spans all known classes of natural and synthetic compounds. It has not only hindered our treatment of infections but also dramatically reshaped drug discovery, yet its origins have not been systematically studied. Soil-dwelling bacteria produce and encounter a myriad of antibiotics, evolving corresponding sensing and evading strategies. They are a reservoir of resistance determinants that can be mobilized into the microbial community. Study of this reservoir could provide an early warning system for future clinically relevant antibiotic resistance mechanisms.
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A screening study of the presence of metallo-β-lactamases (IMP and VIM types and SPM-1) in isolates from different nonhospital sources was conducted, and it revealed the presence of blaVIM-2, associated with the In58 class 1 integron, in two unrelated Pseudomonas aeruginosa strains from aquatic habitats. The results suggest that the hospital setting was the possible origin of these blaVIM-2-carrying strains.
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In the wake of the findings that Antarctic krills concentrate heavy metals at ppm level, (Yamamoto et al. 1987), the Antarctic waters from the Indian side were examined for the incidence of metal and antibiotic-resistant bacteria during the austral summer (13th Indian Antarctic expedition) along the cruise track extending from 50 degrees S and 18 degrees E to 65 degrees S and 30 degrees E. The bacterial isolates from these waters showed varying degrees of resistance to antibiotics (Chloramphenicol, ampicillin, streptomycin, tetracycline and kanamycin) and metals (K(2)CrO(4), CdCl(2), ZnCl(2) and HgCl(2)) tested. Of the isolates screened, about 29% and 16% were resistant to 100 ppm of cadmium and chromium salt respectively. Tolerance to lower concentration (10 ppm) of mercury (Hg) was observed in 68% of the isolates. Depending on the antibiotics the isolates showed different percentage of resistance. Multiple drug and metal-resistance were observed. High incidence of resistance to both antibiotics and metals were common among the pigmented bacterial isolates. Increased resistance decreased the ability of bacteria to express enzymes. The results reiterate previous findings by other researchers that the waters of southern ocean may not be exempt from the spread of metal and antibiotic-resistance.
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Antimicrobials are used in large quantities in human and veterinary medicine. Their environmental occurrence is of particular concern due to the potential spread and maintenance of bacterial resistance. After intake by the organisms, the unchanged drug and its metabolized forms are excreted and enter wastewater treatment plants where they are mostly incompletely eliminated, and are therefore eventually released into the aquatic environment. The reliable detection of several antimicrobials in different environmental aqueous compartments is the result of great improvements achieved in analytical chemistry. This article provides an overview of the more outstanding analytical methods based on liquid chromatography tandem mass spectrometry, developed and applied to determine antimicrobial residues and metabolites present in surface, waste, and ground waters.
The occurrence of sulfonamide and macrolide antimicrobials, as well as trimethoprim, was investigated in conventional activated sludge treatment. Average daily loads in untreated wastewater correlated well with those estimated from annual consumption data and pharmacokinetic behavior. Considerable variations were found during a day, and seasonal differences seem to occur for the macrolides, probably caused by a higher consumption of these substances in winter. The most predominant macrolide and sulfonamide antimicrobials were clarithromycin and sulfamethoxazole, respectively. In the case of sulfamethoxazole, the main human metabolite, N4-acetylsulfamethoxazole, was included as an analyte, accounting for up to 86% of the total load in untreated wastewater. The results obtained illustrate the importance of considering retransformable substances, for example human metabolites, when investigating the behavior and fate of pharmaceuticals. Average concentrations of sulfapyridine, sulfamethoxazole, trimethoprim, azithromycin, and clarithromycin in activated sludge ranged between 28 and 68 microg/kg of dry weight. Overall the sorption to activated sludge was shown to be low for the investigated antimicrobials, with estimated sorption constants for activated sludge below 500 L/kg. Elimination in activated sludge treatment was found to be incomplete for all investigated compounds. In final effluents, the median concentrations for sulfamethoxazole and clarithromycin were 290 and 240 ng/L, respectively.
There is growing concern that metal contamination functions as a selective agent in the proliferation of antibiotic resistance. Documented associations between the types and levels of metal contamination and specific patterns of antibiotic resistance suggest that several mechanisms underlie this co-selection process. These co-selection mechanisms include co-resistance (different resistance determinants present on the same genetic element) and cross-resistance (the same genetic determinant responsible for resistance to antibiotics and metals). Indirect but shared regulatory responses to metal and antibiotic exposure such as biofilm induction also represent potential co-selection mechanisms used by prokaryotes. Metal contamination, therefore, represents a long-standing, widespread and recalcitrant selection pressure with both environmental and clinical importance that potentially contributes to the maintenance and spread of antibiotic resistance factors.
Veterinary antibiotics are widely used at concentrated animal feeding operations (CAFOs) to prevent disease and promote growth of livestock. However, the majority of antibiotics are excreted from animals in urine, feces, and manure. Consequently, the lagoons used to store these wastes can act as reservoirs of antibiotics and antibiotic-resistant bacteria. There is currently no regulation or control of these systems to prevent the spread of these bacteria and their genes for antibiotic resistance into other environments. This study was conducted to determine the disinfection potential of chlorine, ultraviolet light and ozone against swine lagoon bacteria. Results indicate that a chlorine dose of 30 mg/L could achieve a 2.2-3.4 log bacteria reduction in lagoon samples. However, increasing the dose of chlorine did not significantly enhance the disinfection activity due to the presence of chlorine-resistant bacteria. The chlorine resistant bacteria were identified to be closely related to Bacillus subtilis and Bacillus licheniformis. A significant percentage of lagoon bacteria were not susceptible to the four selected antibiotics: chlortetracycline, lincomycin, sulfamethazine and tetracycline (TET). However, the presence of both chlorine and TET could inactivate all bacteria in one lagoon sample. The disinfection potential of UV irradiation and ozone was also examined. Ultraviolet light was an effective bacterial disinfectant, but was unlikely to be economically viable due to its high energy requirements. At an ozone dose of 100 mg/L, the bacteria inactivation efficiency could reach 3.3-3.9 log.
Microbial communities play an important role in stream ecosystem processes, such as breakdown of senescent leaf litter, and as a primary nutritional source for detritivorous macroinvertebrates. Antibiotics may affect stream microbial communities and associated ecosystem processes, especially because recent stream and river monitoring programs have indicated the presence of antibiotics downstream of wastewater treatment plants. In the current study, effects of chronic exposure to the fluoroquinolone antibiotic ciprofloxacin (Cipro) were examined on stream microbial community-level physiological profiles and growth indices of detritivorous amphipods (Gammarus spp.) and caddisflies (Lepidostoma liba). Microcosm experiments were conducted using stream sediments and water, senesced leaf material (Acer saccharum), and macroinvertebrates. A shift in function of leaf-associated microbial communities (based on carbon source utilization) was observed for samples exposed to 100 microg/L of Cipro for 12 d compared to control and treatments exposed to 1 and 10 microg/L of Cipro. This was attributable to carbohydrate substrates, which had 2.7- to 3.5-fold lower microbial respiration than the lower concentrations and control (p < 0.001). For detritivores, Gammarus spp. condition index did not differ among control, 0.1, and 1.0 microg/L treatments after 30-d exposures (p > 0.05). Similarly, L. liba growth rate did not vary among control, 10, and 100 microg/L treatments after 45-d exposures (p > 0.05). These results suggest that Cipro may affect leaf-associated microbial communities, but at concentrations four orders of magnitude above those detected in streams. However, effects of the antibiotic on growth and condition of detritivores were not observed. Future work should focus on identifying specific changes in stream microbial communities as a result of Cipro exposure and impacts on other aquatic species.
The accelerated growth of finfish aquaculture has resulted in a series of developments detrimental to the environment and human health. The latter is illustrated by the widespread and unrestricted use of prophylactic antibiotics in this industry, especially in developing countries, to forestall bacterial infections resulting from sanitary shortcomings in fish rearing. The use of a wide variety of antibiotics in large amounts, including non-biodegradable antibiotics useful in human medicine, ensures that they remain in the aquatic environment, exerting their selective pressure for long periods of time. This process has resulted in the emergence of antibiotic-resistant bacteria in aquaculture environments, in the increase of antibiotic resistance in fish pathogens, in the transfer of these resistance determinants to bacteria of land animals and to human pathogens, and in alterations of the bacterial flora both in sediments and in the water column. The use of large amounts of antibiotics that have to be mixed with fish food also creates problems for industrial health and increases the opportunities for the presence of residual antibiotics in fish meat and fish products. Thus, it appears that global efforts are needed to promote more judicious use of prophylactic antibiotics in aquaculture as accumulating evidence indicates that unrestricted use is detrimental to fish, terrestrial animals, and human health and the environment.