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Open AccessArticle

Evolution of BACON Domain Tandem Repeats in crAssphage and Novel Gut Bacteriophage Lineages

1
Theoretical Biology and Bioinformatics, Science4 Life, Utrecht University, 3584 CH Utrecht, The Netherlands
2
Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, 2629 HZ Delft, The Netherlands
3
Centre for Molecular and Biomolecular Informatics, Radboud Institute for Molecular Life Sciences, Radboud University Medical Centre, 6525 GA Nijmegen, The Netherlands
*
Author to whom correspondence should be addressed.
Viruses 2019, 11(12), 1085; https://doi.org/10.3390/v11121085 (registering DOI)
Received: 31 October 2019 / Revised: 17 November 2019 / Accepted: 19 November 2019 / Published: 21 November 2019
(This article belongs to the Special Issue Computational Biology of Viruses: From Molecules to Epidemics)
The human gut contains an expanse of largely unstudied bacteriophages. Among the most common are crAss-like phages, which were predicted to infect Bacteriodetes hosts. CrAssphage, the first crAss-like phage to be discovered, contains a protein encoding a Bacteroides-associated carbohydrate-binding often N-terminal (BACON) domain tandem repeat. Because protein domain tandem repeats are often hotspots of evolution, BACON domains may provide insight into the evolution of crAss-like phages. Here, we studied the biodiversity and evolution of BACON domains in bacteriophages by analysing over 2 million viral contigs. We found a high biodiversity of BACON in seven gut phage lineages, including five known crAss-like phage lineages and two novel gut phage lineages that are distantly related to crAss-like phages. In three BACON-containing phage lineages, we found that BACON domain tandem repeats were associated with phage tail proteins, suggestive of a possible role of these repeats in host binding. In contrast, individual BACON domains that did not occur in tandem were not found in the proximity of tail proteins. In two lineages, tail-associated BACON domain tandem repeats evolved largely through horizontal transfer of separate domains. In the third lineage that includes the prototypical crAssphage, the tandem repeats arose from several sequential domain duplications, resulting in a characteristic tandem array that is distinct from bacterial BACON domains. We conclude that phage tail-associated BACON domain tandem repeats have evolved in at least two independent cases in gut bacteriophages, including in the widespread gut phage crAssphage. View Full-Text
Keywords: Bacteroides-associated carbohydrate-binding often N-terminal domain; BACON domain; protein domain tandem arrays; bacteriophage; gut virome; crAssphage; metagenomics; phage tail-associated protein domains; genome evolution Bacteroides-associated carbohydrate-binding often N-terminal domain; BACON domain; protein domain tandem arrays; bacteriophage; gut virome; crAssphage; metagenomics; phage tail-associated protein domains; genome evolution
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de Jonge, P.A.; von Meijenfeldt, F.A.B.; van Rooijen, L.E.; Brouns, S.J.J.; Dutilh, B.E. Evolution of BACON Domain Tandem Repeats in crAssphage and Novel Gut Bacteriophage Lineages. Viruses 2019, 11, 1085.

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