Divergent properties and phylogeny of cyanobacterial 5‐<i>enol</i>‐pyruvyl‐shikimate‐3‐phosphate synthases: evidence for horizontal gene transfer in the <i>Nostocales</i>

Forlani, Giuseppe; Bertazzini, Michele; Barillaro, Donatella; Rippka, Rosmarie

doi:10.1111/nph.13022

Cited by 12 publications

(11 citation statements)

References 44 publications

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“…Another possibility is that they possess a glyphosate-tolerant EPSP synthase. In fact, based on the susceptibility to the herbicide, EPSP synthase has been classified into two groups: class I EPSP synthases from plants and bacteria that are sensitive to the phosphonate, and class II that is of bacterial origin and shows a higher tolerance to glyphosate [ 84 ]. Whether the species we examined in this study possess different types of EPSP synthases warrants further investigation.…”

Section: Discussionmentioning

confidence: 99%

Differential Growth Responses of Marine Phytoplankton to Herbicide Glyphosate

Lin

2016

PLoS ONE

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Glyphosate is a globally popular herbicide to kill weeds and its wide applications may lead to accumulation in coastal oceans as a source of phosphorus (P) nutrient or growth inhibitor of phytoplankton. We studied the physiological effects of glyphosate on fourteen species representing five major coastal phytoplankton phyla (haptophyta, bacillariophyta, dinoflagellata, raphidophyta, and chlorophyta). Based on growth responses to different concentrations of glyphosate under contrasting dissolved inorganic phosphorus (DIP) conditions, we found that phytoplankton species could be classified into five groups. Group I (Emiliania huxleyi, Skeletonema costatum, Phaeodactylum tricornutum) could utilize glyphosate as sole P-source to support growth in axenic culture, but in the presence of DIP, they were inhibited by both 36-μM and 360-μM glyphosate. Group II (Karenia mikimotoi, Prorocentrum minimum, Dunaliella tertiolecta, Symbiodinium sp., Heterosigma akashiwo and Alexandrium catenella) could not utilize glyphosate as sole P-source to support growth, and in the presence of DIP growth was not affected by 36-μM but inhibited by 360-μM glyphosate. Glyphosate consistently enhanced growth of Group III (Isochrysis galbana) and inhibited Group IV (Thalassiosira weissflogii, Thalassiosira pseudonana and Chattonella marina) regardless of DIP condition. Group V (Amphidinium carterae) exhibited no measurable response to glyphosate regardless of DIP condition. This grouping is not congruent with the phylogenetic relationships of the phytoplankton species suggesting functional differentiation driven by environmental pressure. We conclude that glyphosate could be used as P-source by some species while is toxic to some other species and yet has no effects on others. The observed differential effects suggest that the continued use of glyphosate and increasing concentration of this herbicide in the coastal waters will likely exert significant impact on coastal marine phytoplankton community structure.

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Section: Discussionmentioning

confidence: 99%

Differential Growth Responses of Marine Phytoplankton to Herbicide Glyphosate

Lin

2016

PLoS ONE

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“…It has been proved that cyanobacteria play a major role in nitrogen, carbon and phosphorus cycling in nature (Forlani et al 2015 ). However, the strains that utilize aminophosphonates seem using these compounds as nutrients, rather as a source of phosphorus, than nitrogen.…”

Section: Discussionmentioning

confidence: 99%

Glyphosate dose modulates the uptake of inorganic phosphate by freshwater cyanobacteria

Drzyzga

Lipok

2017

J Appl Phycol

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The usefulness of glyphosate [N-(phosphonomethyl)glycine] as a source of nutritive phosphorus for species of halophilic cyanobacteria has been postulated for years. Our results indicate a stimulating effect of glyphosate on the growth of four out of five examined freshwater species, Anabaena variabilis (CCALA 007), Chroococcus minutus (CCALA 055), Fischerella cf. maior (CCALA 067) and Nostoc cf. muscorum (CCALA 129), in a manner dependent on the applied concentration. The most significant stimulation was observed at a dose of 0.1 mM glyphosate. The decrease in the amount of phosphonate, which correlated with microbial growth, demonstrated that glyphosate may play an important role in cyanobacterial nourishment. Surprisingly, the consumption of organic phosphorus did not start when concentrations of inorganic phosphate (PO4 3−) had fallen dramatically; instead, the assimilation of both types of phosphorus occurred simultaneously. The greatest decrease in the amount of glyphosate was observed during the first week. The uptake of the standard nutrient-phosphate (PO4 3−), was strongly dependent on the xenobiotic concentration. When a concentration of 0.1 mM glyphosate was used, the consumption of phosphate decreased in favour of glyphosate assimilation. Our study revealed for the very first time that the presence of inorganic phosphate significantly enhances the bioavailability of glyphosate. Statistical analysis confirmed that the nutritive usage of glyphosate and the absorption of phosphate are features associated with the herbicide concentration rather than features related to the species of freshwater cyanobacterium. This finding supports the thesis of an important role of organic phosphorus in the formation of cyanobacterial blooms and creates the opportunity of using these cyanobacteria to bind both organic and inorganic forms of phosphorus in microalgal biomasses.

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“…Cells were extracted by a modification of a previously published protocol (Forlani et al ., ). Briefly, Anabaena cultures in the late exponential phase of growth were harvested by centrifugation for 5 min at 3000 g at 4°C.…”

Section: Methodsmentioning

confidence: 97%

Biodegradation of the aminopolyphosphonate DTPMP by the cyanobacterium Anabaena variabilis proceeds via a C–P lyase‐independent pathway

Drzyzga

Forlani

Vermander

et al. 2017

Environmental Microbiology

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Cyanobacteria, the only prokaryotes capable of oxygenic photosynthesis, play a major role in carbon, nitrogen and phosphorus global cycling. Under conditions of increased P availability and nutrient loading, some cyanobacteria are capable of blooming, rapidly multiplying and possibly altering the ecological structure of the ecosystem. Because of their ability of using non-conventional P sources, these microalgae can be used for bioremediation purposes. Under this perspective, the metabolization of the polyphosphonate diethylenetriaminepenta(methylenephosphonic) acid (DTPMP) by the strain CCALA 007 of Anabaena variabilis was investigated using P NMR analysis. Results showed a quantitative breakdown of DTPMP by cell-free extracts from cyanobacterial cells grown in the absence of any phosphonate. The identification of intermediates and products allowed us to propose a unique and new biodegradation pathway in which the formation of (N-acetylaminomethyl)phosphonic acid represents a key step. This hypothesis was strengthened by the results obtained by incubating cell-free extracts with pathway intermediates. When Anabaena cultures were grown in the presence of the phosphonate, or phosphorus-starved before the extraction, significantly higher biodegradation rates were found.

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Divergent properties and phylogeny of cyanobacterial 5‐enol‐pyruvyl‐shikimate‐3‐phosphate synthases: evidence for horizontal gene transfer in the Nostocales

Cited by 12 publications

References 44 publications

Differential Growth Responses of Marine Phytoplankton to Herbicide Glyphosate

Differential Growth Responses of Marine Phytoplankton to Herbicide Glyphosate

Glyphosate dose modulates the uptake of inorganic phosphate by freshwater cyanobacteria

Biodegradation of the aminopolyphosphonate DTPMP by the cyanobacterium Anabaena variabilis proceeds via a C–P lyase‐independent pathway

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