Gamma-Mobile-Trio systems define a new class of mobile elements rich in bacterial defensive and offensive tools

Abstract

Bacteria are found in ongoing conflicts with rivals and predators, which lead to an evolutionary arms race and the development of innate and adaptive immune systems. Although diverse bacterial immunity mechanisms have been recently identified, many remain unknown, and their dissemination within bacterial populations is poorly understood. Here, we describe a widespread genetic element, defined by the Gamma-Mobile-Trio (GMT) proteins, that serves as a mobile bacterial weapons armory. We show that GMT islands have cargo comprising various combinations of secreted antibacterial toxins, anti-phage defense systems, and secreted anti-eukaryotic toxins. This finding led us to identify four new anti-phage defense systems encoded within GMT islands and reveal their active domains and mechanisms of action. We also find the phage protein that triggers the activation of one of these systems. Thus, we can identify novel toxins and defense systems by investigating proteins of unknown function encoded within GMT islands. Our findings imply that the concept of 'defense islands' may be broadened to include other types of bacterial innate immunity mechanisms, such as antibacterial and anti-eukaryotic toxins that appear to stockpile with anti-phage defense systems within GMT 'weapon islands'.

Multi-conflict islands are a widespread trend withinSerratiaspp

“…More recently, a less conservative analysis of defence islands content evidenced that these regions often show a high degree of plasticity and that anti-phage systems are frequently neighbouring other resistance factors, such as stress genes, antibiotic resistance, and virulence factors 20,48,49 . Importantly, in Vibrio spp., Mahata et al highlighted GMT mobile islands as the first example of co-localisation of anti-phage systems with T6SS-dependent effectors 49 .…”

“…More recently, a less conservative analysis of defence islands content evidenced that these regions often show a high degree of plasticity and that anti-phage systems are frequently neighbouring other resistance factors, such as stress genes, antibiotic resistance, and virulence factors 20,48,49 . Importantly, in Vibrio spp., Mahata et al highlighted GMT mobile islands as the first example of co-localisation of anti-phage systems with T6SS-dependent effectors 49 . In this study, through the analysis of Serratia genomes, we show that this phenomenon is widespread to other defence islands and encompasses several types of offensive and anti-bacterial tools, including colicins, bacteriocins and Cdi systems (Figure 1,2 and Figure S3).…”

“…The type of defence arsenal carried is highly variable even within the same genus 3,18 . An interesting emerging trend suggests that in some genera, including Salmonella and Vibrio , defence hotspots frequently carry a mixed cargo 20,21 . In Salmonella, genomic hotspots carry a variable cargo of anti-phage systems, antibiotic resistance genes and virulence factor 20 .…”

“…In Salmonella, genomic hotspots carry a variable cargo of anti-phage systems, antibiotic resistance genes and virulence factor 20 . Similarly, the gamma-mobile-trio (GMT) islands, initially discovered in Vibrio parahaemolyticus , represents the first reported example of co-localisation of anti-phage systems and Type VI Secretion System (T6SS)-mediated anti-bacterial effectors 21 . Nevertheless, the ratio of anti-phage and anti-bacterial modules of GMT islands exhibit a genus-specific variation 21 .…”

“…Similarly, the gamma-mobile-trio (GMT) islands, initially discovered in Vibrio parahaemolyticus , represents the first reported example of co-localisation of anti-phage systems and Type VI Secretion System (T6SS)-mediated anti-bacterial effectors 21 . Nevertheless, the ratio of anti-phage and anti-bacterial modules of GMT islands exhibit a genus-specific variation 21 . The marked diversity observed in genomic hotspots, flanking genes, and substantial variation in cargo genes across different bacterial species highlights the importance for targeted investigations of these islands within specific genera.…”