JB Accepts, published online ahead of print on 6 November 2009

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J. Bacteriol. doi:10.1128/JB.01174-09
Copyright (c) 2009, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Genomic and biological analysis of phage Xfas53 and related prophages of Xylella fastidiosa

Elizabeth J. Summer, Christopher J. Enderle, Stephen J. Ahern, Jason J. Gill, Cruz P. Torres, David N. Appel, Mark C. Black, Ry Young, and Carlos F. Gonzalez^*

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128; Department of Plant Pathology and Microbiology, Texas A&M University, College, Station, TX 77843-2132; Texas AgriLife Research and Extension Center, Uvalde, TX 78801-6205

^* To whom correspondence should be addressed. Email: cf-gonzalez{at}tamu.edu.

We report the plaque propagation and genomic analysis of Xfas53, a temperate phage of Xylella fastidiosa. Xfas53 was isolated from supernatants of X. fastidiosa strain 53 and forms plaques on the sequenced strain Temecula. Xfas53 forms short-tailed virions, morphologically similar to podophage P22. The 36.7 kb genome is predicted to encode 45 proteins. The Xfas53 terminase and structural genes are related at a protein and gene order level to P22. The left arm of the Xfas53 genome has over 90% nucleotide identity to multiple prophage elements of the sequenced X. fastidiosa strains. This arm encodes proteins involved in DNA metabolism, integration and lysogenic control. In contrast to Xfas53, each of these prophages encode head and DNA packaging proteins related to the siphophage lambda and tail morphogenesis proteins related to those of myophage P2. Therefore, it appears that Xfas53 was formed by recombination between a widespread family of X. fastidiosa P2-related prophage elements and a podophage distantly related to phage P22. The lysis cassette of Xfas53 is predicted to encode a pinholin, a SAR endolysin, and Rz and Rz1 equivalents. The holin gene encodes a pinholin and appears to be subject to an unprecedented degree of negative regulation at both the level of expression, with rho-independent transcriptional termination and RNA structure-dependent translational repression, and at the level of holin function, with two upstream translational starts predicted to encode antiholin products. A notable feature of Xfas53 and related prophages is the presence of 220 to 390 nucleotide degenerate tandem direct repeats encoding putative DNA binding proteins. Additionally, each phage encodes at least two BroN-domain containing proteins possibly involved in lysogenic control. Xfas53 exhibits unusually slow adsorption kinetics, possibly an adaptation to the confined niche of its slow-growing host.