Metabolic arsenal of giant viruses: Host hijack or self-use?

Author:

Brahim Belhaouari Djamal1,Pires De Souza Gabriel Augusto1,Lamb David C2,Kelly Steven L2,Goldstone Jared V3,Stegeman John J3ORCID,Colson Philippe14,La Scola Bernard14,Aherfi Sarah14ORCID

Affiliation:

1. Microbes, Evolution, Phylogeny and Infection (MEPHI), UM63, Institut de Recherche pour le Développement (IRD), IHU Méditerranée Infection, Marseille, France, Aix-Marseille Université

2. Faculty of Medicine, Health and Life Sciences, Institute of Life Science, Swansea University

3. Biology Department, Woods Hole Oceanographic Institution

4. Assistance Publique - Hôpitaux de Marseille (AP-HM)

Abstract

Viruses generally are defined as lacking the fundamental properties of living organisms in that they do not harbor an energy metabolism system or protein synthesis machinery. However, the discovery of giant viruses of amoeba has fundamentally challenged this view because of their exceptional genome properties, particle sizes and encoding of the enzyme machinery for some steps of protein synthesis. Although giant viruses are not able to replicate autonomously and still require a host for their multiplication, numerous metabolic genes involved in energy production have been recently detected in giant virus genomes from many environments. These findings have further blurred the boundaries that separate viruses and living organisms. Herein, we summarize information concerning genes and proteins involved in cellular metabolic pathways and their orthologues that have, surprisingly, been discovered in giant viruses. The remarkable diversity of metabolic genes described in giant viruses include genes encoding enzymes involved in glycolysis, gluconeogenesis, tricarboxylic acid cycle, photosynthesis, and β-oxidation. These viral genes are thought to have been acquired from diverse biological sources through lateral gene transfer early in the evolution of Nucleo-Cytoplasmic Large DNA Viruses, or in some cases more recently. It was assumed that viruses are capable of hijacking host metabolic networks. But the giant virus auxiliary metabolic genes also may represent another form of host metabolism manipulation, by expanding the catalytic capabilities of the host cells especially in harsh environments, providing the infected host cells with a selective evolutionary advantage compared to non-infected cells and hence favoring the viral replication. However, the mechanism of these genes' functionality remains unclear to date.

Funder

Royal Society

Woods Hole Center for Oceans and Human Health

National Institutes of Health

National Science Foundation

Agence Nationale de la Recherche

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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