Assessing the activity of different plant-derived molecules and potential biological nitrification inhibitors on a range of soil ammonia- and nitrite-oxidizing strains

Abstract

ABSTRACT The use of biological nitrification inhibitors (BNIs) holds a great potential to effectively reduce nitrogen losses from agroecosystems and conforms with the current move toward ecological-intensified agriculture. Knowledge of the activity of BNIs to soil nitrifiers is limited and is generally based on a single Nitrosomonas europaea bioassay. We determined the in vitro activity of multiple plant-derived compounds as BNIs such as (i) root-derived compounds [sakuranetin, methyl 3-(4-hydroxyphenyl)-propionate (MHPP), and zeanone]; (ii) other phytochemicals (caffeic, quinic, chlorogenic, and shikimic acids); and (iii) analogs of statins (simvastatin), triazoles (1-butyl-4-propyl-triazole, 1,4-dibutyltriazole), and zeanone (2-methoxy-1,4-naphthoquinone) on distinct soil-derived ammonia-oxidizing bacteria (AOB) ( Nitrosospira multiformis and Nitrosomonas europaea ), ammonia-oxidizing archaea (AOA) ( Candidatus Nitrosotalea sinensis and Candidatus Nitrosocosmicus franklandianus), and a nitrite-oxidizing bacterium (NOB) ( Nitrobacter sp.). Our results indicate that AOA were more sensitive than AOB to BNIs. Sensitivity within the AOA group was BNI dependent, unlike AOB, for which N. multiformis was consistently more sensitive than N. europaea . Several compounds were inhibitory to Nitrobacter sp. with MHPP and caffeic acid being more potent against NOB compared to the ammonia-oxidizing strains, an observation with potential implications for soil quality and productivity. Overall, zeanone was the most potent ΒNI against ammonia oxidizers, while caffeic acid was the most potent BNI against Nitrobacter sp. We provide pioneering evidence for the activity range of multiple BNIs on soil nitrifiers, stress the need for revisiting the biological screening systems currently used for BNI determination, and advocate for a more thorough monitoring of the impact of BNI candidates on a range of target and non-target microorganisms. IMPORTANCE Synthetic nitrification inhibitors are routinely used with nitrogen fertilizers to reduce nitrogen losses from agroecosystems, despite having drawbacks like poor efficiency, cost, and entry into the food chain. Plant-derived BNIs constitute a more environmentally conducive alternative. Knowledge on the activity of BNIs to soil nitrifiers is largely based on bioassays with a single Nitrosomonas europaea strain which does not constitute a dominant member of the community of ammonia-oxidizing microorganisms (AOM) in soil. We determined the activity of several plant-derived molecules reported as having activity, including the recently discovered maize-isolated BNI, zeanone, and its natural analog, 2-methoxy-1,4-naphthoquinone, on a range of ecologically relevant AOM and one nitrite-oxidizing bacterial culture, expanding our knowledge on the intrinsic inhibition potential of BNIs toward AOM and highlighting the necessity for a deeper understanding of the effect of BNIs on the overall soil microbiome integrity before their further use in agricultural settings.