Since phosphonic acid was found to be effective against fungal diseases, in particular those caused by oomycetes, the use of its potassium and sodium salts and its ester fosetyl became very popular in agriculture (for reviews see Guest & Grant, 1991; Dann & McLeod, 2021). It was used as a plant strengthening agrochemical, because it enhances the defence systems of the plant against pathogens. In the EU fosetyl-Al, potassium and sodium phosphonate were approved as fungicides in 2007, 2013 and 2014, respectively. With Commission Regulation (EC) 839/2008 maximum residue levels (MRLs) were defined for fosetyl, expressed as the sum of fosetyl, phosphonic acid and their salts, which are based on peer reviews of the pesticide risk assessment of the corresponding active substances by the European Food Safety Authority (EFSA, 2012, 2013 and 2018). With their approval as active plant protection products, phosphonate salts came also into the focus of EU regulation (EC) No 834/2007 on organic production and labelling of organic products and the use of these chemicals is no longer permitted since 2013 in organic agriculture. Residues of phosphonic acid in organic products are interpreted as a possible indication that rules of organic agriculture have been violated. Although the German Association of Organic Processors, Wholesalers and Retailers (BNN, 2023) and the European Organic Certifiers Council (EOCC, 2019) have defined orientation values for phosphonate, above which checks at farm level should be initiated, there is a tendency at EU level to follow a stricter line and to start such investigations already at findings above 0.01 mg/kg, which is the common limit of quantification (LOQ) achieved by laboratories for most food products. Even more affected are products for infant nutrition, as for these a maximum residue level of 0.01 mg/kg applies under EU regulation (EU) No 2016/127. The Biofosf project “Solving phosphite issue in organic fruit and horticultural crops” tested alternative hypotheses to understand the frequent findings of phosphonate in products from organic agriculture and to propose legislative actions (Trinchera et al., 2020). External inputs not allowed in organic farming, contaminations of fertilizers and plant protection products allowed for organic farming with fosetyl and phosphonate, and storage of phosphonate from previous applications in tree crops were identified as the major causes for phosphonic acid in potato, rocket lettuce and pears from field case-studies.
Phosphorus is a highly reactive element and occurs on earth mainly in the oxidized molecular form together with oxygen and hydrogen. Oxidation states vary from −3 to +5, of which the following are important for the topic of this article: −3 in phosphane, +1 in hypophosphorous acid, +3 in phosphonic acid (also called phosphorous acid, which is actually a minor tautomer of phosphonic acid) and +5 in phosphoric acid and its esters.
In the following hypophosphorous, phosphonic and phosphoric acids will be referred to as their dissociated anions phosphinate (also called hypophosphite), phosphonate (also called phosphite, the anion of phosphorous acid) and phosphate, as the acids normally occur in their dissociated forms at neutral pH in biological systems. As recommended by the International Union of Pure and Applied Chemistry (2005), the term phosphonate will be used exclusively for the inorganic compound. The term organophosphonates will be restricted to the organic compounds with C–P bonds (Ternan et al., 1998).
Phosphorus in its highest oxidation state of +5 in phosphoric acid and its esters are essential for the functioning of all biological systems. For example, the sugar-phosphate backbone forms the structural framework of nucleic acids, including DNA and RNA. Organophosphonates are ubiquitous and account for up to 25% of the dissolved organic phosphorus in some natural samples (Pasek et al., 2014). After the introduction of the 31P NMR (nuclear magnetic resonance) spectrometry organophosphonates were detected in numerous organisms including bacteria, protozoa, fungi, invertebrates and plant seeds (Quin and Quin, 2001; Kafarski, 2019; Maciejczyk et al., 2015; Wieczorek et al., 2021). In seeds of carrots, celery and mustard 9.7, 7.9 and 7.4% of the total phosphorus is bound in organophosphonates. The compounds have been furthermore detected in faeces and manure of farm animals (Toor et al., 2005) and in soil (Newman and Tate, 1980).
Organophosphonates are characterized by a carbon-to-phosphorus (C–P) bond, which makes them far more stable against biological degradation than the esters of phosphonic and phosphoric acid (Ternan et al., 1998). Examples of such naturally occurring organophosphonates are 2-aminoethylphosphonic acid, which was the first natural organophosphonate isolated by Horiguchi and Kandatsu (1960) from sheep rumen ciliate protozoa, and methylphosphonate.
Although phosphonate is thermodynamically unstable due to a redox potential of about −690 mV for the oxidation to phosphate, it is kinetically stable due to high energy required to break the P–H bond (Havlin and Schlegel, 2021). Even in oxygenated water oxidation is slow with half-lives of 1000–3000 years, depending on the temperature, and absent the presence of an oxidizing catalyst capable of forming OH radicals (Herschy et al., 2018). Rocks at the magnetite-hematite oxygen fugacity buffer would even preserve phosphonate indefinitely (Pasek et al., 2013). It is primarily oxidized in the environment by microbes to use it as the sole phosphorus source. This widespread ability among microorganisms is a further indication for the ubiquitous and natural occurrence of phosphonate in the environment. Genes coding for the enzymes catalysing the assimilatory phosphonate oxidation were detected in hundreds of microbial isolates from a variety of environments (Figueroa and Coates, 2017). The chemolithotrophic bacterium Desulfotignum phosphitoxidans is even able to use the low redox potential of −690 mV for the phosphonate to phosphate transition as its sole source of energy by transferring the electrons from the phosphorus onto sulphate to form sulfide (Schink et al., 2002). The phosphate (+5) generated either by assimilatory or dissimilatory phosphonate oxidation can be then brought back to the +3 oxidation stage in organophosphonates by the enzyme phosphoenolpyruvate mutase.
The evaluation of analytical results obtained by Eurofins during the last 10 years reveals the widespread occurrence of phosphonate in food of plant origin both from conventional and organic agriculture. Phosphonate was found in over 40% of all samples both from conventional and organic agriculture tested with methods with a LOQ of 0.01 mg/kg, whereas fosetyl was only detected in 1.08% of samples from conventional and 0.07% of samples from organic agriculture. The Biofosf project evaluated the cause of the frequent occurrence of phosphonate findings in food from organic agriculture by field case-studies (Trinchera et al., 2020) and identified external inputs not allowed in organic farming, contaminations of fertilizers and plant protection products allowed for organic farming with fosetyl and phosphonate, and storage of phosphonate from previous applications in tree crops as the major causes for the phosphonate findings. Contaminations and deliberate adulterations of plant protection products and fertilizers with potent synthetic active ingredients are indeed a severe problem in organic agriculture, as experienced in the case of plant strengtheners like Vi-Care, which were adulterated intentionally with the disinfectants didecyldimethylammonium and benzalkonium chloride, DDAC and BAC (BNN, 2012). Foliar fertilizers used in organic banana cultivation in Ecuador frequently contain phosphonate (Cesar Ponce, personal communication). A further source of minor concentrations of phosphonate are seed dressings with fosetyl, which for example proved to be very beneficial against foot and root rot pathogens affecting pea cultivation (Oyarzun et al., 1990).