The evolutionary replacement of restriction-modification by Ssp antiviral systems is associated with the distribution of prophages in the major clonal group of <i>Acinetobacter baumannii</i>

Bacteriophages kill almost half of the world's bacterial cells every day. In response, bacteria have developed anti-phage defense mechanisms that number in the dozens. Individual defense systems are gained and lost by genomes of the same species, depending on their fitness advantage. Thus, the combination of defense systems presented by the individual genomes may differ, and the collection of all of them is what is known as the pan-immune system of the species. Here, we have analyzed thousands of genomes of the bacterium <i>Acinetobacter baumannii</i>, an opportunistic pathogen of humans of great clinical concern, and we have found 81 different defense systems. By analyzing how these systems combine, we have found that more than half of the genomes lack the universal DNA-methylating restriction-modification systems and harbor an alternative innate Ssp system that performs DNA phosphorothioate modification. The presence of one or the other innate system may modulate the evolution of the genomes of this species, causing them to present a different profile of phages integrated into the bacterial genome. In fact, the most widespread strain of this bacterium worldwide, global clone 2, showed an Ssp system as its distinctive feature. We have also observed that the presence of many other defense systems is associated with the presence of a higher number of prophages, which could be because the prophage carries the system, or because the bacterium would not need these systems in environments where the phage is absent.IMPORTANCE<i>Acinetobacter baumannii</i> is a bacterium of great concern in clinical contexts due to the plasticity of its genome and its resistance to antibiotics. Its cells are infected by a multitude of bacteriophages, and the bacterium defends itself with dozens of different defense systems. Here, we have analyzed the complete defensome of thousands of genomes of the species and found that more than half of the genomes do not have universal restriction-modification systems, which are replaced by another innate labeling and restriction system. Furthermore, these genomes belong to the international clone of the bacterium that causes the most concern in hospitals.

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Journal
mBio
Published
2025-08-18
DOI
https://doi.org/10.1128/mbio.02135-25
Primary Topic
Bacteriophages and microbial interactions
Type
article
Field-Weighted Citation Impact
0.00

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article

The evolutionary replacement of restriction-modification by Ssp antiviral systems is associated with the distribution of prophages in the major clonal group of Acinetobacter baumannii

Younes Smani, Antonio Moreno-Rodríguez, Alejandro Rubio, Antonio J. Pérez‐Pulido et al.
mBio
Bacteriophages and microbial interactions
article

The evolutionary replacement of restriction-modification by Ssp antiviral systems is associated with the distribution of prophages in the major clonal group of Acinetobacter baumannii

Younes Smani, Antonio Moreno-Rodríguez, Alejandro Rubio, Antonio J. Pérez‐Pulido, Andrés Garzón
article en

Abstract

Bacteriophages kill almost half of the world's bacterial cells every day. In response, bacteria have developed anti-phage defense mechanisms that number in the dozens. Individual defense systems are gained and lost by genomes of the same species, depending on their fitness advantage. Thus, the combination of defense systems presented by the individual genomes may differ, and the collection of all of them is what is known as the pan-immune system of the species. Here, we have analyzed thousands of genomes of the bacterium <i>Acinetobacter baumannii</i>, an opportunistic pathogen of humans of great clinical concern, and we have found 81 different defense systems. By analyzing how these systems combine, we have found that more than half of the genomes lack the universal DNA-methylating restriction-modification systems and harbor an alternative innate Ssp system that performs DNA phosphorothioate modification. The presence of one or the other innate system may modulate the evolution of the genomes of this species, causing them to present a different profile of phages integrated into the bacterial genome. In fact, the most widespread strain of this bacterium worldwide, global clone 2, showed an Ssp system as its distinctive feature. We have also observed that the presence of many other defense systems is associated with the presence of a higher number of prophages, which could be because the prophage carries the system, or because the bacterium would not need these systems in environments where the phage is absent.IMPORTANCE<i>Acinetobacter baumannii</i> is a bacterium of great concern in clinical contexts due to the plasticity of its genome and its resistance to antibiotics. Its cells are infected by a multitude of bacteriophages, and the bacterium defends itself with dozens of different defense systems. Here, we have analyzed the complete defensome of thousands of genomes of the species and found that more than half of the genomes do not have universal restriction-modification systems, which are replaced by another innate labeling and restriction system. Furthermore, these genomes belong to the international clone of the bacterium that causes the most concern in hospitals.

mBioVol. 16(9)
Centro Andaluz de Biología del Desarrollo (ES), Universidad Pablo de Olavide (ES)
Agencia Estatal de Investigación
Openalex Percentile: Top 79%
Bacteriophages and microbial interactions
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