Strain-Specific Gifsy-1 Prophage Genes Are Determinants for Expression of the RNA Repair Operon during the SOS Response in Salmonella enterica Serovar Typhimurium

Kurasz, Jennifer E; Crawford, Madison C; Porwollik, Steffen; Gregory, Oliver; Tadlock, Katerina R; Balding, Eve C; Weinert, Emily E.; McClelland, Michael; Karls, Anna C.

doi:10.1128/jb.00262-22

Cited by 5 publications

(4 citation statements)

References 49 publications

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“…Finally, three translocated proteins, CbeA, YagB, and YfJZ, are antitoxins characteristically encoded within prophages ( Table 1 ). This finding is of interest given that RecA and the SOS response are known inducers of prophage lytic programs and toxin-antitoxin systems ( 81 , 82 ). Conceivably, translocation of these antitoxins serves to block phage-encoded or other toxins produced as a component of the mating-induced SOS response.…”

Section: Resultsmentioning

confidence: 89%

The F plasmid conjutome: the repertoire of E. coli proteins translocated through an F-encoded type IV secretion system

Al Mamun,

Kissoon,

et al. 2024

mSphere

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Bacterial conjugation systems pose a major threat to human health through their widespread dissemination of mobile genetic elements (MGEs) carrying cargoes of antibiotic resistance genes. Using the Cre Recombinase Assay for Translocation (CRAfT), we recently reported that the IncFV pED208 conjugation system also translocates at least 16 plasmid-encoded proteins to recipient bacteria. Here, we deployed a high-throughput CRAfT screen to identify the repertoire of chromosomally encoded protein substrates of the pED208 system. We identified 32 substrates encoded by the Escherichia coli W3110 genome with functions associated with (i) DNA/nucleotide metabolism, (ii) stress tolerance/physiology, (iii) transcriptional regulation, or (iv) toxin inhibition. The respective gene deletions did not impact pED208 transfer proficiencies, nor did Group 1 (DNA/nucleotide metabolism) mutations detectably alter the SOS response elicited in new transconjugants upon acquisition of pED208. However, MC4100(pED208) donor cells intrinsically exhibit significantly higher SOS activation than plasmid-free MC4100 cells, and this plasmid carriage-induced stress response is further elevated in donor cells deleted of several Group 1 genes. Among 10 characterized substrates, we gained evidence of C-terminal or internal translocation signals that could function independently or synergistically for optimal protein transfer. Remarkably, nearly all tested proteins were also translocated through the IncN pKM101 and IncP RP4 conjugation systems. This repertoire of E. coli protein substrates, here termed the F plasmid “conjutome,” is thus characterized by functions of potential benefit to new transconjugants, diverse TSs, and the capacity for promiscuous transfer through heterologous conjugation systems. IMPORTANCE Conjugation systems comprise a major subfamily of the type IV secretion systems (T4SSs) and are the progenitors of a second large T4SS subfamily dedicated to translocation of protein effectors. This study examined the capacity of conjugation machines to function as protein translocators. Using a high-throughput reporter screen, we determined that 32 chromosomally encoded proteins are delivered through an F plasmid conjugation system. The translocated proteins potentially enhance the establishment of the co-transferred F plasmid or mitigate mating-induced stresses. Translocation signals located C-terminally or internally conferred substrate recognition by the F system and, remarkably, many substrates also were translocated through heterologous conjugation systems. Our findings highlight the plasticity of conjugation systems in their capacities to co-translocate DNA and many protein substrates.

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Section: Resultsmentioning

confidence: 89%

The F plasmid conjutome: the repertoire of E. coli proteins translocated through an F-encoded type IV secretion system

Al Mamun,

Kissoon,

et al. 2024

mSphere

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“…1F). As it appears that oxidative DNA damage activates prophage simultaneously with RNA repair ( 15 ), we investigated whether Gifsy prophage activation caused tRNA cleavage. A strain of S. enterica lacking all three Gifsy prophages failed to induce tRNA Leu cleavage after exposure to H 2 O 2 (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The data so far indicated the presence of a previously uncharacterized nuclease in the Gifsy-1 prophage that can target its bacterial host’s tRNA molecules. We initially focused on the STM14_3218-20 operon within the Gifsy-1 prophage, a locus that is associated with the activation of rtc gene transcription after antibiotic-mediated DNA damage ( 15 ) and that is present in Salmonella Typhimurium strain 14028s but absent in S. Typhimurium strains LT2 or SL1344. Northern blot analyses showed that H 2 O 2 induced tRNA Leu cleavage in S. Typhimurium strains LT2, SL1344—as well as in S. Typhimurium 14028s mutants bearing multiple- or single-gene deletions in the STM14_3218-20 operon—as efficiently as in the WT 14028s strain (fig.…”

Section: Resultsmentioning

confidence: 99%

Prophage terminase with tRNase activity sensitizes Salmonella enterica to oxidative stress

Uppalapati,

Kant,

Liu

et al. 2024

Science

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Phage viruses shape the evolution and virulence of their bacterial hosts. The Salmonella enterica genome encodes several stress-inducible prophages. The Gifsy-1 prophage terminase protein, whose canonical function is to process phage DNA for packaging in the virus head, unexpectedly acts as a transfer ribonuclease (tRNase) under oxidative stress, cleaving the anticodon loop of tRNA Leu . The ensuing RNA fragmentation compromises bacterial translation, intracellular survival, and recovery from oxidative stress in the vertebrate host. S. enterica adapts to this transfer RNA (tRNA) fragmentation by transcribing the RNA repair Rtc system. The counterintuitive translational arrest provided by tRNA cleavage may subvert prophage mobilization and give the host an opportunity for repair as a way of maintaining bacterial genome integrity and ultimately survival in animals.

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“…Furthermore, the identification of the prophages Gifsy-1, Gifsy-2, Fels-1, and Fels-2 in S. Typhimurium has been linked to an adaptative response to stress conditions. 50 Notably, studies have established that the Gifsy prophage family may genetically contribute to the presence of the…”

Section: Discussionmentioning

confidence: 99%

Genomic perspective of Salmonella enterica isolated from farm animals in Sinaloa, Mexico

Campo,

Aguirre-Sanchez,

Irvin

et al. 2024

IJMR

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Farm animals play a crucial role as a primary source of sustenance for human consumption. However continues to be one of the major food-borne pathogens from a public health standpoint. Its persistent global concern surrounding stems from its capability to induce foodborne illnesses. Unraveling the genetic characteristics of this pathogen stands as a pivotal step, shedding light on the intricate biology of and aiming to mitigate its prevalence. Within this context, our study aims to delve into the genomic traits and population structure of Mexican isolates derived from farm animals. We performed next-generation sequencing across 72 genomes. Genomic data was analyzed to determine virulence and antibiotic resistance markers. In addition, a phylogenetic tree and a spanning tree was constructed. The study revealed a diversity of 18 serovars linked to a singular ST, with prominent serovars being Oranienburg, Give, and Saintpaul. Across all isolates, an extensive array of virulence-related genes was identified. Interestingly, 95% of the isolates displayed exclusive resistance to aminoglycosides, while the remaining exhibited multidrug resistance to tetracycline and chloramphenicol. Notably, a substantial prevalence of prophages in the genomes was observed, accounting for 94% and totaling 183 sequences. The serovar Give stood out with the highest number of sequences, featuring Vibrio X29 and Escher RCS47 as the most prevalent phages. This comprehensive analysis provides valuable insights into the intricate world of , paving the way for enhanced understanding and targeted interventions.

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Strain-Specific Gifsy-1 Prophage Genes Are Determinants for Expression of the RNA Repair Operon during the SOS Response in Salmonella enterica Serovar Typhimurium

Abstract: The transcriptional activator RtcR and the RNA repair proteins whose expression it regulates, RtcA and RtcB, are widely conserved in Proteobacteria . In Salmonella Typhimurium 14028s, genotoxic stress activates RtcR to direct RpoN-dependent expression of the rsr-yrlBA-rtcBA operon.

Cited by 5 publications

References 49 publications

The F plasmid conjutome: the repertoire of E. coli proteins translocated through an F-encoded type IV secretion system

The F plasmid conjutome: the repertoire of E. coli proteins translocated through an F-encoded type IV secretion system

Prophage terminase with tRNase activity sensitizes Salmonella enterica to oxidative stress

Genomic perspective of Salmonella enterica isolated from farm animals in Sinaloa, Mexico

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