Evolution of DNA packaging in gene transfer agents

Author:

Esterman Emma S1ORCID,Wolf Yuri I2,Kogay Roman1,Koonin Eugene V2ORCID,Zhaxybayeva Olga13ORCID

Affiliation:

1. Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA

2. National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD 20894, USA

3. Department of Computer Science, Dartmouth College, Hanover, NH 03755, USA

Abstract

Abstract Gene transfer agents (GTAs) are virus-like particles encoded and produced by many bacteria and archaea. Unlike viruses, GTAs package fragments of the host genome instead of the genes that encode the components of the GTA itself. As a result of this non-specific DNA packaging, GTAs can transfer genes within bacterial and archaeal communities. GTAs clearly evolved from viruses and are thought to have been maintained in prokaryotic genomes due to the advantages associated with their DNA transfer capacity. The most-studied GTA is produced by the alphaproteobacterium Rhodobacter capsulatus (RcGTA), which packages random portions of the host genome at a lower DNA density than usually observed in tailed bacterial viruses. How the DNA packaging properties of RcGTA evolved from those of the ancestral virus remains unknown. To address this question, we reconstructed the evolutionary history of the large subunit of the terminase (TerL), a highly conserved enzyme used by viruses and GTAs to package DNA. We found that RcGTA-like TerLs grouped within viruses that employ the headful packaging strategy. Because distinct mechanisms of viral DNA packaging correspond to differences in the TerL amino acid sequence, our finding suggests that RcGTA evolved from a headful packaging virus. Headful packaging is the least sequence-specific mode of DNA packaging, which would facilitate the switch from packaging of the viral genome to packaging random pieces of the host genome during GTA evolution.

Funder

Dartmouth College to E.S.E.: Sophomore Research Scholarship, James O. Freedman Presidential Scholarship

Thomas B. Roos Memorial Fund Fellowship

Kaminsky Undergraduate Research Award

National Institutes of Health to E.S.E.

Simons Foundation Investigator in Mathematical Modeling of Living Systems

National Science Foundation

Intramural Research Program of the U.S. National Institutes of Health (National Library of Medicine) to Y.I.W. and E.V.K.

Publisher

Oxford University Press (OUP)

Subject

Virology,Microbiology

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