Viral infection collapses intracytoplasmic membrane integrity and autotrophic metabolism in ammonia-oxidizing Nitrosomonas europaea

Abstract

Ammonia-oxidizing bacteria (AOB) catalyze the first and rate-limiting step of nitrification. They are essential for nitrogen cycling in engineered and natural environments, yet little is known about their viruses or the consequences of phage infection for host physiology. Here, we report the isolation and characterization of a novel lytic bacteriophage, vB_NeuP-Nir1 (Nir1), infecting the model AOB Nitrosomonas europaea. Phage Nir1 was highly virulent, ceased ammonia oxidation within hours, and caused complete lysis of host populations even at multiplicities of infection as low as 10-6. Electron microscopy revealed drastic host cell remodeling during infection, including pronounced cell bloating and large-scale disintegration of intracytoplasmic membranes. Integrated transcriptomic and metabolomic analyses showed that loss of these ATP and reducing equivalent generating membrane systems was accompanied by signatures of compromised lipid homeostasis and collapse of autotrophic CO2 fixation. In parallel, Nir1 infection induced metabolic rewiring of the host, including upregulation of uptake systems for nucleic acids, amino acids, and small organic compounds, increased expression of iron acquisition and putative iron-dependent respiratory components, as well as accumulation of metabolites associated with membrane breakdown and stabilization of viral DNA. Together, these results provide the first detailed mechanistic insight into phage-induced host modulation in a chemolithoautotrophic nitrifier. Our study establishes the Nir1-N. europaea system as a model for investigating virus-host interactions in AOB and lays the foundation for assessing the role of phages in shaping nitrification and nitrogen cycling in engineered and natural ecosystems.