A giant virus infecting the amoeboflagellate Naegleria

• Published in: Nature communications 2024-04, Vol.15 (1), p.3307-13, Article 3307
• Main Authors: Arthofer, Patrick, Panhölzl, Florian, Delafont, Vincent, Hay, Alban, Reipert, Siegfried, Cyran, Norbert, Wienkoop, Stefanie, Willemsen, Anouk, Sifaoui, Ines, Arberas-Jiménez, Iñigo, Schulz, Frederik, Lorenzo-Morales, Jacob, Horn, Matthias
• Format: Article
• Language: English
• Subjects: 14/32; 14/63; 45; 45/23; 631/326/596; 692/699/255/1715; Adaptation; Algae; Apoptosis; BASIC BIOLOGICAL SCIENCES; Electron microscopy; Fluorescence in situ hybridization; Genes; Genome, Viral - genetics; Giant Viruses - classification; Giant Viruses - genetics; Giant Viruses - isolation & purification; Giant Viruses - physiology; Giant Viruses - ultrastructure; Heat shock proteins; Humanities and Social Sciences; Humans; Lethality; Life Sciences; Meningoencephalitis; Metagenomics; multidisciplinary; Naegleria; Naegleria - genetics; Naegleria - virology; Naegleria fowleri - genetics; Naegleria fowleri - isolation & purification; parasitic infection; Pathogens; Phylogeny; Primary amebic meningoencephalitis; Proteomics; Science; Science (multidisciplinary); virology; Viruses
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-47308-2

Giant viruses ( Nucleocytoviricota ) are significant lethality agents of various eukaryotic hosts. Although metagenomics indicates their ubiquitous distribution, available giant virus isolates are restricted to a very small number of protist and algal hosts. Here we report on the first viral isolate that replicates in the amoeboflagellate Naegleria . This genus comprises the notorious human pathogen Naegleria fowleri , the causative agent of the rare but fatal primary amoebic meningoencephalitis. We have elucidated the structure and infection cycle of this giant virus, Catovirus naegleriensis (a.k.a. Naegleriavirus, NiV), and show its unique adaptations to its Naegleria host using fluorescence in situ hybridization, electron microscopy, genomics, and proteomics. Naegleriavirus is only the fourth isolate of the highly diverse subfamily Klosneuvirinae , and like its relatives the NiV genome contains a large number of translation genes, but lacks transfer RNAs (tRNAs). NiV has acquired genes from its Naegleria host, which code for heat shock proteins and apoptosis inhibiting factors, presumably for host interactions. Notably, NiV infection was lethal to all Naegleria species tested, including the human pathogen N. fowleri . This study expands our experimental framework for investigating giant viruses and may help to better understand the basic biology of the human pathogen N. fowleri . This is the first report on a virus infecting the amoeboflagellate Naegleria , including the lethal human pathogen N. fowleri . The new virus isolate, Catovirus naegleriensis (Naegleriavirus, NiV), shows hallmarks of giant viruses (Nucleocytoviricota) and unique adaptations to its protist host.