Nitric Oxide Accumulation: The Evolutionary Trigger for Phytopathogenesis

Abstract

Many publications highlight the importance of nitric oxide (NO) in plant–bacteria interactions, either in the promotion of health and plant growth or in pathogenesis. However, the role of NO in the signaling between bacteria and plants and in the fate of their interaction, as well as the reconstruction of their interactive evolution, remains largely unknown. Despite the complexity of the evolution of life on Earth, we explore the hypothesis that denitrification and aerobic respiration were responsible for local NO accumulation, which triggered primordial antagonistic biotic interactions, namely the first phytopathogenic interactions. N-oxides, including NO, could globally accumulate via lightning synthesis in the early anoxic ocean and constitute pools for the evolution of denitrification, considered an early step of the biological nitrogen cycle. Interestingly, a common evolution may be proposed for components of denitrification and aerobic respiration pathways, namely for NO and oxygen reductases, a theory compatible with the presence of low amounts of oxygen before the great oxygenation event (GOE), which was generated by Cyanobacteria. During GOE, the increase in oxygen caused the decrease of Earth’s temperature and the consequent increase of oxygen dissolution and availability, making aerobic respiration an increasingly dominant trait of the expanding mesophilic lifestyle. Horizontal gene transfer was certainly important in the joint expansion of mesophily and aerobic respiration. First denitrification steps lead to NO formation through nitrite reductase activity, and NO may further accumulate when oxygen binds NO reductase, resulting in denitrification blockage. The consequent transient NO surplus in an oxic niche could have been a key factor for a successful outcome of an early denitrifying prokaryote able to scavenge oxygen by NO/oxygen reductase or by an independent heterotrophic aerobic respiration pathway. In fact, NO surplus could result in toxicity causing “the first disease” in oxygen-producing Cyanobacteria. We inspected in bacteria the presence of sequences similar to the NO-producing nitrite reductase nirS gene of Thermus thermophilus, an extreme thermophilic aerobe of the Thermus/Deinococcus group, which constitutes an ancient lineage related to Cyanobacteria. In silico analysis revealed the relationship between the presence of nirS genes and phytopathogenicity in Gram-negative bacteria.

The Double-Faced Role of Nitric Oxide and Reactive Oxygen Species in Solid Tumors

“…Nitric oxide (NO) is included as a universal signal in diverse biosystems, and plays a key role in communication both inside the cell and between the cell and the environment [22]. This feature was developed through evolution and was influenced by many factors.…”

“…This feature was developed through evolution and was influenced by many factors. Due to its high chemical reactivity, the list of target molecules that may undergo significant biological and functional modifications in response to NO is very long [22]. The biological activities of NO are realized through cyclin guanosine monophosphate (cGMP)-dependent and cGMP-independent routes.…”

Alkaloids, Nitric Oxide, and Nitrite Reductases: Evolutionary Coupling as Key Regulators of Cellular Bioenergetics with Special Relevance to the Human Microbiome

“…Consistent with the physiological demands of developing biological processes, limited abiotic generation of NO from N2 and O2 via lightning discharge [ 6 ] was superseded by multiple enzymatic pathways of nitrification and denitrification by primordial microbial systems. Interestingly, evolutionary transition of largely anaerobic to microbial-based aerobic nitrogen cycles by the late Archean period approximately 2.5 billion years ago may have preceded significant atmospheric O2 accumulation generated by Cyanobacteria before the great oxygenation event at the end of Proterozoic period [ 7 , 8 ].…”

“…Evolutionary development of major enzymatic components of microbial denitrification and aerobic respiration drives NO and N2O formation by nitrite reductase (NIR) and nitric oxide reductase (NOR) activities, respectively [ 8 ]. Furthermore, co-evolution of denitrification and aerobic respiratory complexes within hybrid prokaryotic respiratory chains provide strong putative evidence for the operationally-dependent amplification of the chemical diversity of NO as a pluripotent effector molecule within eukaryotic biological systems [ 9 ], including its potential role as a chemical mediator of microbial symbioses with diverse eukaryotic hosts [ 10 ].…”

A Molecular Line Survey around Orion at Low Frequencies with the MWA

“…Laboratory experiments have created enamines (precursors to amines) with deuterated Formic Acids in a neutral medium (Himmele et al 1979), suggesting that the tentative detections of deuterated formic acid and nitric oxide may point to the production of amines within the Orion molecular cloud. NO is also of particular interest as it is thought to be critically important in primitive life on Earth (Feelisch & Martin 1995;Santana et al 2017).…”