Symbiosis of a P2‐family phage and deep‐sea Shewanella putrefaciens

Summary Almost all bacterial genomes harbour prophages, yet it remains unknown why prophages integrate into tRNA‐related genes. Approximately 1/3 of Shewanella isolates harbour a prophage at the tmRNA (ssrA) gene. Here, we discovered a P2‐family prophage integrated at the 3′‐end of ssrA in the deep‐...

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Bibliographic Details
Published in:Environmental microbiology 2019-11, Vol.21 (11), p.4212-4232
Main Authors: Liu, Xiaoxiao, Tang, Kaihao, Zhang, Dali, Li, Yangmei, Liu, Zhe, Yao, Jianyun, Wood, Thomas K., Wang, Xiaoxue
Format: Article
Language:English
Subjects:
Aquatic Organisms - genetics
Bacterial genomes
Bacteriophage P2 - physiology
Biofilms
Complementation
COX protein
Defects
Disruption
Genes
Genome, Bacterial - genetics
Genomes
Growth
Harbors
Harbours
Microbiological strains
Phages
Prophages
Prophages - genetics
Proteins
Recombination
Rep protein
RNA, Bacterial - genetics
Seawater
Shewanella putrefaciens - genetics
Shewanella putrefaciens - virology
Symbionts
Symbiosis
Symbiosis - genetics
TmRNA
tRNA
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Summary:Summary Almost all bacterial genomes harbour prophages, yet it remains unknown why prophages integrate into tRNA‐related genes. Approximately 1/3 of Shewanella isolates harbour a prophage at the tmRNA (ssrA) gene. Here, we discovered a P2‐family prophage integrated at the 3′‐end of ssrA in the deep‐sea bacterium S. putrefaciens. We found that ~0.1% of host cells are lysed to release P2 constitutively during host growth. P2 phage production is induced by a prophage‐encoded Rep protein and its excision is induced by the Cox protein. We also found that P2 genome excision leads to the disruption of wobble base pairing of SsrA due to site‐specific recombination, thus disrupting the trans‐translation function of SsrA. We further demonstrated that P2 excision greatly hinders growth in seawater medium and inhibits biofilm formation. Complementation with a functional SsrA in the P2‐excised strain completely restores the growth defects in seawater medium and partially restores biofilm formation. Additionally, we found that products of the P2 genes also increase biofilm formation. Taken together, this study illustrates a symbiotic relationship between P2 and its marine host, thus providing multiple benefits for both sides when a phage is integrated but suffers from reduced fitness when the prophage is excised.
ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.14781