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Vol. 7(32), pp. 4084-4090, 9 August, 2013
DOI: 10.5897/AJMR12.2302
ISSN 1996-0808 ©2013 Academic Journals
http://www.academicjournals.org/AJMR
African Journal of Microbiology Research
Review
Metabolism and degradation of glyphosate in aquatic
cyanobacteria: A review
K. K. I. U. Arunakumara1, Buddhi Charana Walpola2 and Min-Ho Yoon2*
1Department of Crop Science, Faculty of Agriculture, University of Ruhuna, Sri Lanka.
2Department of Bio-Environmental Chemistry, College of Agriculture and Life Sciences, Chungnam National University,
Korea.
Accepted 28 July, 2013
Use of glyphosate (N-phosphonomethylglycine), a broad-spectrum, non-selective, post-emergence
herbicide has been increased steadily with the introduction of genetically modified glyphosate-resistant
crops. Increased reliance on herbicides for suppressing weeds and aggressive marketing have also
contributed substantially to rising demand for glyphosate. Degradation of glyphosate was basically
done by soil microorganisms; however, once the herbicide reached to the aquatic systems,
cyanobacterial strains were reported to be involved in the process of biodegradation. Upon glyphosate
exposure, a remarkable tolerance was reported in many strains, where cell proliferation was found to be
completely unaffected by the herbicide at the concentration of micromolar to millimolar range.
However, the mechanism through which cyanobacteria exhibit the tolerance seemed to be widely varied
and species-dependent. Carrier-independent uptake of glyphosate has been suggested as the
resistance mechanism at micromolar level concentrations. Presence of resistant form of the target
enzyme EPSP (5-enolpyruvylshikimate-3-phosphate) and the ability of some strains to metabolize
glyphosate have also been reported to be responsible for the tolerance. A remarkable ability to degrade
glyphosate has been identified from some cyanobacterial strains such as Spirulina spp. where
degradative pathway was however reported to be different from those exhibited in other bacteria.
Exploitation of cyanobacteria in biological treatments of waste water contaminated with glyphosate has
not yet been reported, mainly due to lack of research evidence on as to how cyanobacteria deal with
biodegradation of glyphosate under field conditions.
Key words: Glyphosate, cyanobacteria, biodegradation, biological treatments.
GLYPHOSATE USAGE AND MODE OF ACTION
Glyphosate (N-phosphonomethylglycine), a broad-
spectrum, non-selective, post-emergence herbicide is
widely used in suppressing annual and perennial weeds
in agricultural lands, ornamental and residential gardens
and in aquatic systems (Walpola et al., 2007; Lipok et al.,
2010). The herbicide is also used in silviculture for con-
trolling undesirable competing vegetation that may emerge
after harvesting of high-yield coniferous plantations.
Some glyphosate based herbicides specifically formu-
lated to be used as aquatic herbicides are employed
extensively to control noxious aquatic weeds and algal
blooms (Siemering et al., 2008). Due to its widespread
usage over the years, glyphosate is now considered to be
the most studied organophosphonate (Lipok et al., 2009).
Though, different chemical formulations are commercially
available, glyphosate is generally formulated in its form
*Corresponding author. E-mail: mhyoon@cnu.ac.kr. Tel: +82-42-821-6733. Fax: +82-42-823-9241.
Figure 1. Glyphosate molecule.
of isopropylamine salt (IPA salt) (Figure 1). However,
commercial preparations (for example, Roundup®) were
reported to be more toxic than glyphosate alone (Tsui
and Chu, 2003; Cedergreen and Streibig, 2005; Sobrero
et al., 2007). Agricultural use of glyphosate greatly
expanded with the development of minimum and no-
tillage cultivation systems, where application of herbi-
cides prior to planting became a standard practice
(Walpola et al., 2007). No-tillage practice is found to be
rapidly adopted around the world (Altieri and Pengue,
2006) as it improves soil quality avoiding organic matter
lost (Bayer et al., 2006) and water evaporation and
protects soil from erosion (Bollinger et al., 2006). Further-
more, this practice is economically affordable for a wide
range of farming communities.
Use of glyphosate further expanded with the intro-
duction of genetically modified glyphosate-resistant crops
(Woodburn, 2000), which mainly include soybean, maize,
cotton, canola and sugar beet (Duke, 2011). However, as
time progressed, less sensitive and herbicide-resistant
weed species are reported to be evolved (Pérez and
Kogan, 2003; Powles, 2008; Binimelis et al., 2009)
forcing farmers to increase the average rate of glypho-
sate application per unit area. The global increase in
usage of glyphosate is also associated with aggressive
marketing, as well as with the increased reliance on
herbicides for controlling weeds (Pengue, 2005). Glypho-
sate does possess slow mode of action, which ensures
distribution of the herbicide throughout the plant before
appearing the symptoms. In fact, once enter to plants,
metabolic degradation of glyphosate takes place slowly
or sometimes no degradation at all, thus highly effective
for many plant species. As reported by Cerdeira and
Duke (2006), the shikimate pathway is blocked by
glyphosate through inhibition of 5-enolpyruvyl-shikimate-
3-phosphate synthase (EPSPS). Conse-quently, protein
synthesis is haltered due to deregulation of the shikimate
pathway and inhibition of the formation of aromatic amino
acids tryptophan, tyrosine and phenylalanine (Duke et al.,
2003). As symptoms, growth is inhibited immediately
after application, followed by foliar chlorosis and necrosis
is shown within 4 to 7 days in highly susceptible species
(Senseman, 2007). However, it may take 2 to 3 weeks to
display symptoms in susceptible species.
Arunakumara et al. 4085
As a post emergence herbicide, glyphosate is recom-
mended at doses ranging 0.21 and 4.2 kg a.i. per ha
depending on the use (Vencill, 2002). In most of the
agricultural lands, the application dose is generally over 1
kg per ha (Cerdeira and Duke, 2006).
SOIL EXPOSURE AND CONTAMINATION OF
AQUATIC SYSTEMS
Upon exposure, glyphosate is usually assumed to be
tightly adsorbed to soil, though its persistence in soil
depends on the climate and soil characteristics (Perez et
al., 2007). However, Helander et al. (2012) reported that
glyphosate is neither entirely no immediately degraded in
soils, where degradation is mainly done by soil micro-
organisms. Despite glyphosate is found to be toxic to
several microbes (Busse et al., 2001), growth enhance-
ment is also reported from some microbes (Kremer and
Means, 2009). Thus, the presence of glyphosate can
result in alterations in soil microbial community structure
(Lancaster et al., 2010). As stated by Helander et al.
(2012), the effects of glyphosate and its main degradation
product aminomethylphosphonic acid (AMPA) on soil
microorganisms and biological interactions can be com-
plex and multidirectional. As of the published literature,
the average half-life of glyphosate in soil varies between
2 and 197 days (WHO, 1988; Giesey et al., 2000); thus, a
typical field half-life of 47 days has been suggested
(Vencill, 2002). Due to the mobility of glyphosate in soil,
contamination of groundwater could also be possible
through leaching. However, such leaching is reported to
be restricted to some special climatic, soil and spraying
conditions (Vereecken, 2005; Borggaard and Gimsing,
2008; Laitinen, 2006). In this context, a considerable rate
of glyphosate leaching has been reported in very coarse
(gravelly) materials with limited retention capacity
(Torstensson et al., 2005). As reported by Kjaer et al.
(2005) and Candela et al. (2010), excessive irrigation or
rainfall immediately after application could also be res-
ponsible for increasing risk of leaching. Though not
significant, terrestrial applications of glyphosate can also
result in contamination of aquatic systems through acci-
dental offsite movement in herbicide spray drift, or
through surface run-off (Abrantes et al., 2009). Unaccep-
ted habits such as washing and cleaning the tanks of the
fumigation machines in streams and adjacent water
bodies near cultivation fields may also result in reaching
glyphosate to the water bodies.
In waters, glyphosate is found to be chemically stable
because it does not undergo photochemical degradation
(Lipok et al., 2010). As stated by Scribner et al. (2007),
glyphosate and AMPA are among the frequently reported
pesticides detected in water-pollution monitoring. While
degradation, AMPA is formed by other phosphonate
compounds also (Kolpin et al., 2006; Botta et al., 2009),
thus glyphosate could not be considered as the main
4086 Afr. J. Microbiol. Res.
source of AMPA (Trass and Smit, 2003). Pérez et al.
(2007) elaborating the possible impacts of glyphosate on
the structure of the phytoplankton and periphyton com-
munities in fresh water, reduction in total micro- and
nanophytoplankton has been reported. Glyphosate could
have a direct effect on the periphytic colonization of
substrata (Vera et al., 2010). Therefore, it is obvious that
non-target periphyton and phytoplankton communities in
aquatic ecosystems could be affected by the toxicity of
glyphosate. The application of glyphosate in fresh water
systems may result in shifting the community from gly-
phosate-sensitive green algae and diatoms to glyphosate
-tolerant cyanobacteria (Saxton et al., 2011). Indirect
effects via the eutrophication potential of glyphosate
degradation should also be taken into account; thus,
overall functioning of the aquatic ecosystems and the
basis of food webs may be potentially affected by gly-
phosate.
Alterations in microbial community structure upon gly-
phosate exposure have been described in marine envi-
ronments also (Stachowski-Haberkorn et al., 2008). In
water, the average half-life of glyphosate may vary from a
few days to 91 days (Tomlin, 2006).
EFFECT OF GLYPHOSATE ON CYANOBACTERIA
Cyanobacteria, a highly diverse group of prokaryotic
microorganisms exhibiting oxygenic photosynthesis has
gained high recognition as the most efficient solar energy
harvesters among all the living organisms (Kulasooriya,
2011). They could be found in all most all kind of habitats
including extreme terrestrial and aquatic environments,
thus account for a major proportion of the total phyto-
plankton biomass (Arunakumara, 2012). Due to their
remarkable ecophysiological adaptation, they are able to
cope with different kind of stress conditions (Lee et al.,
2003; Barton et al., 2004; Dyhrman et al., 2006; Parikh et
al., 2006). However, they have not yet been fully exploi-
ted for biological treatment of polluted waters, and only
scanty information is available on as to how cyanobac-
teria participates in the process of biodegradation of
chemical pollutants. Six cyanobacterial strains (Anabaena
sp., Arthrospira fusiformis, Leptolyngbya boryana,
Microcystis aeruginosa, Nostoc punctiforme, Spirulina
platensis) were employed in a laboratory investigation to
examine the basis of their resistance to glyphosate
(Forlani et al., 2008). Remarkable tolerance was observed
in all the strains, where cell proliferation was found to be
completely unaffected by the herbicide in the micromolar
to millimolar range. Quite interestingly, A. fusiformis and
S. platensis have not showed any significant increase in
their doubling time even at the highest dose tested (10
mM). Lipok et al. (2007) conducted a laboratory investi-
gation with a mixed culture of Spirulina spp. and reported
that the growth was not affected with the addition of
glyphosate at low concentration (0.2 mM). They have ob-
observed a short growth cycle (maximal cell density at 5
to 6 days after the inoculation). However, as concentra-
tion increased over 20 mM, a significant reduction in
growth was observed in a dose-dependent manner.
Explaining their results with M. aeruginosa, Lo´pez-
Rodas et al. (2007) reported that rare spontaneous pre-
selective mutations could assist in surviving the strain
against glyphosate stress. Furthermore, they quoted that
such mutants can be expected only if appropriate genetic
variability is available within the species. Their comment
is in line with Whitton (2002), who reported formation of a
glyphosate resistance population of M. aeruginosa from
cells with slightly different morphology. Whole-cell system
with S. platensis cells grown in standard medium was
employed in elucidating the ability of cyanobacteria to
metabolize glyphosate (Forlani et al., 2008). Based on
the findings, they stated that the possible act of carrier -
independent uptake of glyphosate at micromolar level
concentrations which results in remarkable tolerance to
the herbicide. Therefore, at micromoler level concen-
trations, cell impermeability attributed largely to the tole-
rance mechanism exhibited in S. platensis. According to
them, the initial tolerance up to 20 mM is in line with the
previous reports (Sikha and Singh, 2004; Singh and
Datta, 2005) on varying resistance of cyanobacteria to
this herbicide.
Powell et al. (1992) reported that tolerance of Anabaena
variabilis ATCC 29413 is related to the presence of a
resistant form of the target enzyme EPSP, which is
consistence with the findings of Forlani et al. (2008) for
Anabaena spp and N. punctiforme. Based on this, it is
quite reasonable to consider that the presence of an
insensitive variant of the target enzyme as a biochemical
basis of in vivo tolerance. However, they have observed
a significant growth inhibition at levels at which enzyme
activity was completely unaffected, thus effect of in vivo
may be higher than that of in vitro. Having considered all
these reports, Forlani et al. (2008) suggested that
tolerance is attributed to several mechanisms work in a
cooperative manner. Making similar remarks, Vera et al.
(2010) reported that cyanobacteria may resist glyphosate
by different strategies. Among them, the overproduction
of EPSP synthase or the production of a glyphosate-
tolerant enzyme (Powell et al., 1991) and degradation of
glyphosate and use it as a phosphorus source (Forlani et
al., 2008) are still considered to be dominant, despite the
variations reported among different species. However,
contrary to this, Pewell et al. (1991) have reported that no
evidence of glyphosate degradation could be observed
with Synechocystis PCC 6803 and A. variabilis ATCC
29413 though the species exhibited a high degree of
tolerance to glyphosate. According to them, toxicity
differed with the type of formulations (Roundup >
isopropylamine salt > free acid) and correlated with their
rates of uptake.
Taking all aforementioned into account, it is quite rea-
sonable to state that aquatic systems may not frequently
Arunakumara et al. 4087
Table 1. The effect of glyphosate on several cyanobacterial strains.
Strain
Concentration
Remark
Reference
Synechocystis Sauvageau (PCC
6803)
0.5 - 20 mM
Confirmed tolerance even at 20 mM
Powell et al. (1991)
Anabaena variabilis Kutz (ATCC
29413)
S. (Arthrospira) platensis
0.07 mM
Confirmed tolerance
Lipok et al. (2010)
Arthrospira fusiformis
Confirmed tolerance
Nostoc punctiforme
Confirmed tolerance
Anabaena catenula
Sensitive
Synechocistis aquatilis
Sensitive
Microcystis aeruginosa
Sensitive
Leptolynbya boryana
sensitive
Spirulina spp
0.2 - 20 mM
Confirmed tolerance up to 20 mM, thereafter
significant growth reduction
Lipok et al. (2007)
Anabaena sp. ATCC 27347 (PCC
7120)
0.01 - 10mM
Confirmed tolerance in the micromolar to millimolar
range
Forlani et al. (2008)
Arthrospira fusiformis CCALA 023
Leptolyngbya boryana ATCC 27894
(PCC 6306)
Microcystis aeruginosa PCC 7941
(CCALA 106)
Nostoc punctiforme ATCC 29133
(PCC 73102)
Spirulina platensis C1 (PCC 9438)
Microcystis aeruginosa
0 - 110 ppm
Sensitive, growth was totally inhibited at 110 ppm
(0.7 mM)
Lo´ pez-Rodas et al.
(2007)
receive glyphosate at a concentration enough for sup-
pressing cyanobacterial growth (Forlani et al., 2008),
because, though applied at a recommended dose ran-
ging 0.21 and 4.2 kg a.i. per ha depending on the use
(Vencill, 2002), substantial amount of off-targeted gly-
phosate is adsorbed to soil particles, minimizing signi-
ficant leaching or removal by means of surface run-off,
which might ultimately reach to neighbouring waters.
Table 1 summarizes the effect of glyphosate on several
cyanobacterial strains.
DEGRADATION OF GLYPHOSATE
The presence of chemically and thermally stable C-P
bond, a characteristic feature of glyphosate (Singh and
Walker, 2006) is a matter of frequent concern, because,
the C-P linkage is found to be heavily resistant to non-
biological degradation in the environment (Hayes et al.,
2000). As per the published literature, biodegradation of
glyphosate is believed to be done basically by soil
microorganisms and the process can be described under
two different metabolic pathways (Duke, 2011). One
process involves in splitting the glyphosate C-N bond by
the action of glyphosate oxidoreductase (GOX) enzyme
to produce aminomethylphosphonic acid (AMPA) and
glyoxylate (Schuette, 1998). In fact, glyoxylate is not only
a metabolite derived of glyphosate degradation, but also
a plant endogenous metabolite involved in different
metabolic pathways (Rojano-Delgado et al., 2010). By
the action of the enzyme C-P lyase, AMPA, the other
main metabolite is degraded to methylamine, which ulti-
mately generates formaldehyde by the action of methyl-
amine dehydrogenase enzyme (Lerbs et al., 1990).
Formaldehyde quickly reacts with water and/or hydroxyl
radicals to form methanol. Thus, the ultimate yield of the
glyphosate degradation may contain carbon dioxide,
phosphate, ammonia and methanol (Araujo et al., 2003).
In the second pathway, sarcosine (N-methyl-glycine) is
yielded through direct degradation of gly-phosate by the
action of C-P lyase enzyme (Dick and Quinn, 1995;
Schuette, 1998; Kafarski et al., 2000). The sarcosine can
further be degraded into amino acids such as glycine,
serine, cysteine, methionine and histidine (Pipke et al.,
1987). Based on the aforementioned, Rojano-Delgado et
4088 Afr. J. Microbiol. Res.
al. (2010) stated that the availability of these metabolites
and their relative percentage can be used in assessing
glyphosate metabolism in plants. In addition to the two
common pathways aforementioned, Pizzul et al. (2009)
reported that ligninolytic enzymes of soil microflora do
have the ability to cleave the C-P bond of glyphosate. In
the presence of manganese oxide, cleavage of C-P bond
of glyphosate could also be witnessed non-enzymatically
though it has not often been reported in soil (Barrett and
McBride, 2005). A large number of soil microorganisms
such as bacteria, fungi, actinomycetes and some uniden-
tified microbes are reported to be involved in glyphosate
degradation (Borggaard and Gimsing, 2008). Further-
more, as reported by Gimsing et al. (2004) for Pseudomonas
spp., the degradation rate is strongly correlated with the
population size of soil microbes.
With regard to degradation in aqueous mediums, Lipok
et al. (2007) concluding their findings with mixed culture
of Spirulina spp, reported that the species exhibited a
remarkable ability to degrade glyphosate, where the rate
of glyphosate disappearance from the medium was inde-
pendent of its initial concentration. They suggested that
the degradative pathway for glyphosate in Spirulina spp.
might differ from those exhibited in other bacteria.
According to them, occurrence of herbicide metabolism in
Spirulina is evident, because, the species can grow in a
medium containing phosphonate as the only source of
phosphorus, where the rate of herbicide transformation
was found to be depended upon the cells‟ phosphorus
status. In fact, Lipok et al. (2009) re-confirmed the ability
of the cyanobacterium S. platensis and bacterium Strep-
tomyces lusitanus to catalyze glyphosate metabolism.
According to Forlani et al. (2008), four cyanobacterial
strains (Anabaena sp., L. boryana, M. aeruginosa and N.
punctiforme) out of the six strains studied were able to
use the glyphosate as the only source of phosphorus.
Dyhrman et al. (2006) too stated that the existence of
phosphorous-dependent glyphosate transformation with
marine cyanobacterium Trichodesmium erythraeum.
Glyphosate as a source of nitrogen for microorganism
was also reported (Klimek et al., 2001) with Penicillium
chrysogenum and then with Alternaria alternate (Lipok et
al., 2003). However, reports on the utilization of gly-
phosate as a source of nitrogen by cyanobacteria are not
yet available in the literature. Elaborating their findings
with cyanobacterium A. variabilis, Ravi and Balakumar
(1998) reported that extracellular phosphatases are able
to hydrolyze the C-P bond of glyphosate; however, this
claim has not been reiterated so far by the other authors.
Forlani et al. (2008) based on their results, stated that
extracellular phosphatases seems unlikely to contribute
any substantial scale to glyphosate degradation. As
described earlier, different steps are reported to be invol-
ved in the process of glyphosate degradation in different
strains of microorganisms. Some of them in fact can
utilize glyphosate as a source of nutrient. In this regard,
cyanobacterial strains which possess the ability to use
this phosphonate as a source of phosphorus is of
practically significance, because, such strains could
effectively be employed in treating the problematic
waters.
CONCLUSION
It is quite obvious that the use of glyphosate has brought
impressive economical benefits, in particular, through the
enhanced agricultural productivity. However, due to high
percentage of applied glyphosate is often reported to be
deposited on non-target areas, contamination of soil and
water is inevitable. Under this background, frequent
assessments on the impacts to non-target organisms are
of prime importance. However, the vast majority of the
present investigations dealing with the impact of gly-
phosate on aquatic organisms and mechanism involved
in degradation are based on laboratory bioassays.
Furthermore, toxicity studies are often targeted on indi-
vidual strains, because, such findings assist in assessing
the direct impacts of herbicide on the organisms of
concern. However, generation of remediation strategies
for contaminated waters, merely based on such findings
would not be advisable. Thus, field studies conducted in
natural environments are encouraged as they could come
up with much broader understanding as to how cyano-
bacteria cope with glyphosate toxicity.
REFERENCES
Abrantes N, Pereira R, de Figueiredo DR, Marques CR, Pereira MJ,
Gonçalves F (2009). A whole sample toxicity assessment to evaluate
the sub-lethal toxicity of water and sediment elutriates from a lake
exposed to diffuse pollution. Environ. Toxicol. 24: 259-270.
Altieri MA, Pengue W (2006). GM soybean: Latin America‟s new
colonizer. Seedling, January issue, 2006.
Araujo ASF, Monteiro RTR, Abarkeli RB (2003). Effect of glyphosate on
the microbial activity of two Brazilian soils. Chemosphere 52: 799-
804.
Arunakumara KKIU (2012). Bioaccumulation of Metals in
Cyanobacteria: Effects on Growth, Morphology and Pigment
Contents. LAP LAMBERT Academic Publishing, AG & Co KG.
Barrett KA, McBride MB (2005). Oxidative degradation of glyphosate
and aminomethylphosphonate by manganese oxide. Environ. Sci.
Technol. 39: 9223-9228.
Barton JW, Kurtiz T, O‟Connor LE, Ma CY, Maskarinee MP, Davison
BH (2004). Reductive transformation of methyl parathion by
cyanobacterium Anabaena sp., strain PCC 7120. Appl. Microb. Cell
Physiol. 65: 330-335.
Bayer C, Lovato T, Dieckow, J, Zanatta JA, Mielniczuk J (2006). A
method for estimating coefficients of soil organic matter dynamics
based on long-term experiments. Soil Tillage Res. 91: 217-226.
Binimelis R, Pengue W, Monterroso I (2009). „„Transgenic treadmill”:
Responses to the emergence and spread of glyphosate-resistant
Johnson grass in Argentina. Geoforum 40: 623-633.
Bollinger A, Magid J, Jorge T, Amado C, Neto FS, Ribeiro M, Calegari
A, Ralisch R, Neergaard A (2006). Taking stock of the Brazilian
“Zero-Till Revolution”: A review of landmark research and farmer
practice. Adv. Agron. 91: 47-110.
Borggaard OK, Gimsing AL (2008). Fate of glyphosate in soil and the
possibility of leaching to ground and surface waters. Pest Manag. Sci.
64: 441-456.
Botta F, Lavison G, Couturier G, Alliot F, Moreau-Guigon E, Fauchon N,
Guery B, Chevreuil M, Blanchoud H (2009). Transfer of glyphosate
and its degradate AMPA to surface waters through urban sewerage
systems. Chemosphere 77: 133-139.
Busse MD, Ratcliff AW, Shestak CJ, Powers RF (2001). Glyphosate
toxicity and the effects of long-term vegetation control on soil
microbial communities. Soil Biol. Biochem. 33: 1777-1789.
Candela L, Caballero J, Ronen D (2010). Glyphosate transport
through weatheredgranite s oils under irrigated and non -
irrigated conditions - Barcelona, Spain. Sci. Total Environ. 408:
2509-2516.
Cedergreen N, Streibig JC (2005). The toxicity of herbicides to non-
target aquatic plants and algae: assessment of predictive factors and
hazard. Pest Manag. Sci. 61: 1152-1160.
Cerdeira AL, Duke SO (2006). The current status and environmental
impacts of glyphosate-resistant crops: A review. J. Environ. Qual. 35:
1633-1658.
Dick RE, Quinn JP (1995). Glyphosate-degrading isolates from
environmental samples: occurrence and pathway of degradation.
Appl. Microbiol. Biotechnol. 43: 545-550.
Duke SO (2011). Glyphosate degradation in glyphosate-resistant and -
susceptible crops and weeds. J. Agric. Food Chem. 59: 5835-5841.
Duke SO, Baerson SR, Rimando AM (2003). Herbicides: Glyphosate.
In: Plimmer JR, Gammon DW, Ragsdale NN (eds.) Encycl. of
Agrochemicals. Available at http://www.mrw.
interscience.wiley.com/eoa/articles/agr119/frame.html. John Wiley &
Sons, New York, NY, USA.
Dyhrman ST, Chapell PD, Haley ST, Moffett JW, Orchard ED,
Waterbury JB (2006). Phosphonate utilization by the globally
important marine diazotroph Trichodesmium. Nature 439: 68-71.
Forlani G, Pavan M, Gramek M, Kafarski P, Lipok J (2008). Biochemical
bases for a widespread tolerance of cyanobacteria to the
phosphonate herbicide glyphosate. Plant Cell Physiol. 49: 443-456.
Giesey JP, Dobson S, Solomon KR (2000). Ecotoxicological risk
assessment for Roundup herbicide. Rev. Environ. Contam. Toxicol.
167: 35-120.
Gimsing AL, Borggaard OK, Jacobsen OS, Sørensen AJ (2004).
Chemical and microbiological soil characteristics controlling
glyphosate mineralization in Danish surface soils. Appl. Soil Ecol. 27:
233-242.
Hayes VEA, Ternan NG, McMullan G (2000). Organophosphate
metabolism by a moderately halophilic bacterial isolate. FEMS
Microbiol. Lett. 186: 171-175.
Helander M, Saloniemi I, Saikkonen K (2012). Glyphosate in northern
ecosystems. Trends in Plant Science.
http://dx.doi.org/10.1016/j.tplants.2012.05.008. Assessed on 20th Nov
2012.
Kafarski P, Lejczak B, Forlani G (2000). Biodegradation of pesticides
containing carbon to phosphorus bond. In: Hall JC, Hoagland RE,
Zablotowicz RM (eds) Pesticide biotransformation in plants and
microorganisms. Similarities and divergencies. Washington, DC:
ACS; 2000. pp. 145-163.
Kjaer JP, Olsen P, Ullum M, Grant R (2005). Leaching of glyphosate
and amino-methylphosphonic acid from Danish agricultural field sites.
J. Environ. Qual. 34: 608-620.
Klimek M, Lejck B, Kafarski P, Forlani G (2001). Metaboilism of the
phosphonate herbicide glyphosate by a non-nitrateutilising strain of
Penicillium chrysogenum. Pest. Mang. Sci. 57: 815-821.
Kolpin DW, Thurman EM, Lee EA, Meyer MT, Furlong ET, Glassmeyer
ST (2006). Urban contributions of glyphosate and its degradate
AMPA to streams in the United States. Environ. Sci. Technol. 354:
191-197.
Kremer RJ, Means NE (2009). Glyphosate and glyphosate-resistant
crop interactions with rhizosphere microorganisms. Eur. J. Agron. 31:
153-161.
Kulasooriya SA (2011). Cyanobacteria: Pioneers of Planet Earth.
Ceylon J. Sci. 40: 71-88.
Laitinen P, Siimes K, Eronen L, Rämö S, Welling L, Oinonen S, Mattsoff
L, Ruohonen-Lehto M (2006). Fate of the herbicides glyphosate,
glufosinate- ammonium, phenmedipham, ethofumesate and
metamitron in two Finnish arable soils. Pest Manag. Sci. 62: 473-491.
Arunakumara et al. 4089
Lancaster SH, Hollister EB, Senseman SA, Gentry TJ (2010). Effects of
repeated glyphosate applications on soil microbial community
composition and the mineralization of glyphosate. Pest Manag. Sci.
66: 59‐64.
Lee S, Kim J, Kennedy IR, Park J, Kwon G, Koh S, Kim JE (2003).
Biotransformation of an organochlorine insecticide, endosulfan, by
Anabaena species. J. Agric. Food Chem. 51: 1336-1340.
Lerbs W, Stock M, Parthier B (1990). Physiological aspects of
glyphosate degradation in Alcaligenes sp. strain GL. Arch. Microbiol.
153: 146-150.
Lipok J, Dombrovska L, Wieczorek P, Kafarski P (2003). The ability of
fungi isolated from stored carrot seeds to degrade organo-
phosphonate herbicides. Pesticide in Air, Plant, Soil and water
System (Del Re AAM, Capri E, Padovani L, Trevisan M (eds)
Proceeding of the XII Symposium Pesticide Chemistry, Piacenza,
Italy.
Lipok J, Owsiak T, Młynarz P, Forlani G, Kafarski P (2007). Phosphorus
NMR as a tool to study mineralization of organophosphonates-The
ability of Spirulina spp. to degrade glyphosate. Enzyme Microb.
Technol. 41: 286-291.
Lipok J, Studnik H, Gruyaert S (2010). The toxicity of Roundups 360 SL
formulation and its main constituents: Glyphosate and isopropylamine
towards non-target water photoautotrophs. Ecotoxicol. Environ. Saf.
73: 1681-1688.
Lipok J, Wieczorek D, Jewgin´ ski M, Kafarski P (2009). Prospects of in
vivo 31P NMR method in glyphosate degradation studies in whole
cell system. Enzyme Microb. Technol. 44: 11-16.
Lo´ pez-Rodas V, Flores-Moya A, Maneiro E, Perdigones N, Marva F,
Garcı´a ME, Costas E (2007). Resistance to glyphosate in the
cyanobacterium Microcystis aeruginosa as result of pre-selective
mutations. Evol. Ecol. 21: 535-547.
Parikh A, Shah V, Madamwar D (2006). Cyanobacterial flora from
polluted marine shores. Environ. Monit. Assess. 120: 407-414.
Pengue W (2005). Transgenic crops in Argentina: the ecological and
social debt. Bull. Sci. Technol. Soc. 25: 314-322.
Perez A, Kogan M (2003). Glyphosate-resistant Lolium multiflorum in
Chilean orchards. Weed Res. 43: 12-19.
Pérez GL, Torremorell A, Mugni H, Rodriguez P, Vera MS, do
Nascimento M, Allende L, Bustingorry J, Escaray R, Ferraro M,
Izaguirre I, Pizarro H, Bonetto C, Morris DP, Zagarese H (2007).
Effects of the herbicide Roundup on freshwater microbial commu-
nities: A mesocosm study. Ecol. Appl. 17: 2310-2322.
Pipke R, Amrhein N, Jacob GS, Kishore GM, Schaefer J (1987).
Metabolism of glyphosate in an Arthrobacter sp. GLP-1. Eur. J.
Biochem. 165: 267-273.
Pizzul L, del Pilar Castillo M, Stenst€om J (2009). Degradation of
glyphosate and other pesticides by ligninolytic enzymes. Biodegra-
dation 20: 751-759.
Powell HA, Kerby NW, Rowell P (1991). Natural tolerance of
cyanobacteria to the herbicide glyphosate. New Phytol. 119: 421-426.
Powell HA, Kerby NW, Rowell P, Mousdale DM, Coggins JR (1992).
Purification and properties of a glyphosate-tolerant 5-enol pyruvyl
shikimate 3-phosphate synthase from the cyanobacterium Anabaena
variabilis. Planta 188: 484-490.
Powles SB (2008). Evolved glyphosate-resistant weeds around the
world: lessons to be learnt. Pest. Manag. Sci. 64: 360-365.
Ravi V, Balakumar H (1998). Biodegradation of the C-P bond in
glyphosate by the cyanobacterium Anabaena variabilis L. J. Sci. Ind.
Res. India 57: 790-794.
Rojano-Delgado AM, Ruiz-Jimnez J, Castro MDL, De Prado R (2010).
Determination of glyphosate and its metabolites in plant material by
reversed-polarity CE with indirect absorptiometric detection.
Electrophoresis 31: 1423-1430.
Saxton MA, Morrow EA, Bourbonniere RA, Wilhelm SW (2011).
Glyphosate influence on phytoplankton community structure in Lake
Erie. J. Great Lakes Res. 37: 683-690.
Schuette J (1998). Environmental Fate of Glyphosate; DPR: Sacra-
mento, CA, 1998. p. 13.
Scribner EA, Battaglin WA, Gilliom RJ, Meyer MT (2007). Concentra-
tions of glyphosate, its degradation product, aminomethylphosphonic
acid, and glufosinate in ground- and surface-water, rainfall, and soil
4090 Afr. J. Microbiol. Res.
samples collected in the United States, 2001–06- Scientific
Investigations Report 2007–5122, U.S. Geological Survey, Reston,
Virginia.
Senseman SA (ed) (2007). Herbicide Handbook. 9th ed. Lawrence, KS:
Weed Science Society of America. pp. 243-246.
Siemering G, Hayworth J, Greenfield B (2008). Assessment of potential
herbicide impacts to California aquatic ecosystems. Arch. Environ.
Contam. Toxicol. 55: 415-431.
Sikha DP, Singh S (2004). Influence of glyphosate on photosynthetic
properties of wild type and mutant strains of cyanobacterium
Anabaena doliolum. Curr. Sci. 86: 571-576.
Singh BK, Walker A (2006). Microbial degradation of organophosphorus
compounds. FEMS Microbiol. Rev. 30: 428-471.
Singh S, Datta P (2005). Growth and survival potentials of immobilized
diazotrophic cyanobacterial isolates exposed to common rice field
herbicides. World J. Microbiol. Biotechnol. 21: 441-446.
Sobrero MC, Rimoldi F, Ronco AE (2007). Effects of the glyphosate
active ingredient and a formulation on Lemma gibba L. at different
exoposure levels and assessment endpoints. Bull. Environ. Contam.
Toxicol. 79: 537-543.
Stachowski-Haberkorn S, Becker B, Marie D, Haberkorn H, Coroller L,
de la Broise D (2008). Impact of Roundup on the marine microbial
community, as shown by an in situ microcosm experiment. Aquat.
Toxicol. 89: 232-241.
Tomlin CDS (2006). The Pesticide Manual: A World Compendium, 14th
ed. British Crop Protection Council, Hampshire, UK, 2006. pp. 545-
548.
Torstensson L, Borjesson E, Stenstrom J (2005). Efficiacy and fate of
glyphosate on Swedish railway embankments. Pest Manag. Sci. 6:
881-886.
Trass TP, Smit CE (2003). Environmental risk limits for
aminomethylphosphonic acid (AMPA) RIVM report 601501018/2003.
National Institute of Public Health and the Environment. Bilthoven,
The Netherlands.
Tsui MTK, Chu LM (2003). Aquatic toxicity of glyphosate-based
formulations: comparison between different organisms and the
effects of environmental factors. Chemosphere 52: 1189-1197.
Vencill WK (ed) (2002). Herbicide Handbook, 8th ed. Weed Science
Society of America, Lawrence, KS, 2002. pp. 231-234.
Vera MS, Lagomarsino L, Sylvester M, Pérez GL, Rodriguez P, Mugni
H, Sinistro R, Ferraro M, Bonetto C, Zagares H, Pizarro H (2010).
New evidence of Roundup (glyphosate formulation) impact on
periphyton community and the water quality of freshwater
ecosystems. Ecotoxicology 19: 710-721.
Vereecken H (2005). Mobility and leaching of glyphosate: a review. Pest
Manag. Sci. 61:1139–1151.
Walpola BC, Wanniarachchi SD Liyanage JA (2007). Responses of the
soil microbial biomass carbon to the herbicides propanil and
glyphosate. J. Agric. Sci. 3:122-130.
Whitton BA (2002). Phylum Cyanophyta (Blue Green Algae/
Cyanobacteria). In: John DJ, Whitton BA, Brook AJ (eds) The
freshwater algal flora of the British Isles. An identification guide to
freshwater and terrestrial algae. Cambridge University Press,
Cambridge, UK. pp. 25-122.
WHO (1988). Environmental Health Criteria 159, Toxicological
Evaluations - Glyphosate; International Programme on Chemical
Safety, World Health Organization: Geneva, Switzerland.
Woodburn AT(2000). Glyphosate: production, princing and use
worldwide. Pest Manag. Sci. 56: 309-312.
