Alcaligenes ammonioxydans HO-1 antagonizes Bacillus velezensis via hydroxylamine-triggered population response

Abstract

Antagonism is a common behavior seen between microbes in nature. Alcaligenes ammonioxydans HO-1 converts ammonia to nitrogen under aerobic conditions, which leads to the accumulation of extracellular hydroxylamine (HA), providing pronounced growth advantages against many bacterial genera, including Bacillus velezensis V4. In contrast, a mutant variant of A. ammonioxydans, strain 2-29, that cannot produce HA fails to antagonize other bacteria. In this article, we demonstrate that cell-free supernatants derived from the antagonistic HO-1 strain were sufficient to reproduce the antagonistic behavior and the efficiency of this inhibition correlated strongly with the HA content of the supernatant. Furthermore, reintroducing the capacity to produce HA to the 2-29 strain or supplementing bacterial co-cultures with HA restored antagonistic behavior. The HA-mediated antagonism was dose-dependent and affected by the temperature, but not by pH. HA caused a decline in biomass, cell aggregation, and hydrolysis of the cell wall in exponentially growing B. velezensis bulk cultures. Analysis of differential gene expression identified a series of genes modulating multicellular behavior in B. velezensis. Genes involved in motility, chemotaxis, sporulation, polypeptide synthesis, and non-ribosomal peptide synthesis were all significantly downregulated in the presence of HA, whereas autolysis-related genes showed upregulation. Taken together, these findings indicate that HA affects the population response of coexisting strains and also suggest that A. ammonioxydans HO-1 antagonize other bacteria by producing extracellular HA that, in turn, acts as a signaling molecule.

Hydroxylamine production by Alcaligenes faecalis challenges the paradigm of heterotrophic nitrification

“…71 . Later, NH 2 OH production by A. faecalis was also shown to have antifungal 72,73 and antibacterial 74,75 effects. NH 2 OH secretion could, therefore, be a competitive strategy.…”

“…NH 2 OH secretion could, therefore, be a competitive strategy. In fact, A. faecalis grown in de ned co-cultures had a competitive advantage over its concomitant organisms, which the authors ascribed to the production of NH 2 OH 75 . Furthermore, A.…”

Tapping the Potential of Wastewater Treatment with Direct Ammonia Oxidation (Dirammox)

“…First, the biochemistry of transforming ammonia into NH 2 OH during the Dirammox process remains a mystery and requires further investigation. From a bioenergetics perspective, it is unclear whether the ammonia oxidation process provides extra energy for bacterial growth or serves as a detoxification mechanism, while the accumulation of extracellular hydroxylamine by the genus Alcaligenes provided pronounced growth advantages compared to other bacteria . Additionally, the extent to which the Dirammox process contributes to the global nitrogen balance is unclear.…”

“…From a bioenergetics perspective, it is unclear whether the ammonia oxidation process provides extra energy for bacterial growth or serves as a detoxification mechanism, while the accumulation of extracellular hydroxylamine by the genus Alcaligenes provided pronounced growth advantages compared to other bacteria. 11 Additionally, the extent to which the Dirammox process contributes to the global nitrogen balance is unclear. It is necessary to apply 15 N tracing experiments to accurately quantify a variety of simultaneously occurring gross nitrogen transformation processes, including Dirammox in actual environments.…”

Direct ammonia oxidation (Dirammox) is favored over cell growth in Alcaligenes ammonioxydans HO‐1 to deal with the toxicity of ammonium

“…In this work, we discovered a redistribution phenomenon for nitrogen between the Dirammox and cell growth processes. A. ammonioxydans HO-1 chose the Dirammox process instead of the physiological state with a rapid doubling time and higher biomass during the course of evolution.Recent studies have shown that A. ammonioxydans HO-1 exhibits a pronounced antagonism activity against a wide range of microbes like B. velezensis V4 through the production of extracellular NH 2 OH, a key intermediate of the Dirammox(Gao et al, 2022). Meanwhile, the products of Dirammox, NH 2 OH, could degrade antibiotics(Su et al, 2023) and chemically transform organic micropollutants(Su et al, 2021) to increase bacterial tolerance in complex natural environments.…”